Literature DB >> 28674006

Clusters of calcium release channels harness the Ising phase transition to confine their elementary intracellular signals.

Anna V Maltsev1, Victor A Maltsev2, Michael D Stern3.   

Abstract

Intracellular Ca signals represent a universal mechanism of cell function. Messages carried by Ca are local, rapid, and powerful enough to be delivered over the thermal noise. A higher signal-to-noise ratio is achieved by a cooperative action of Ca release channels such as IP3 receptors or ryanodine receptors arranged in clusters (release units) containing a few to several hundred release channels. The channels synchronize their openings via Ca-induced Ca release, generating high-amplitude local Ca signals known as puffs in neurons and sparks in muscle cells. Despite the positive feedback nature of the activation, Ca signals are strictly confined in time and space by an unexplained termination mechanism. Here we show that the collective transition of release channels from an open to a closed state is identical to the phase transition associated with the reversal of magnetic field in an Ising ferromagnet. Our simple quantitative criterion closely predicts the Ca store depletion level required for spark termination for each cluster size. We further formulate exact requirements that a cluster of release channels should satisfy in any cell type for our mapping to the Ising model and the associated formula to remain valid. Thus, we describe deterministically the behavior of a system on a coarser scale (release unit) that is random on a finer scale (release channels), bridging the gap between scales. Our results provide exact mapping of a nanoscale biological signaling model to an interacting particle system in statistical physics, making the extensive mathematical apparatus available to quantitative biology.

Keywords:  calcium; calcium spark; excitation–contraction coupling; heart; ryanodine receptor

Mesh:

Substances:

Year:  2017        PMID: 28674006      PMCID: PMC5530665          DOI: 10.1073/pnas.1701409114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  28 in total

1.  Termination of cardiac Ca(2+) sparks: an investigative mathematical model of calcium-induced calcium release.

Authors:  Eric A Sobie; Keith W Dilly; Jader dos Santos Cruz; W Jonathan Lederer; M Saleet Jafri
Journal:  Biophys J       Date:  2002-07       Impact factor: 4.033

2.  Sarcoplasmic Reticulum Structure and Functional Properties that Promote Long-Lasting Calcium Sparks.

Authors:  Daisuke Sato; Thomas R Shannon; Donald M Bers
Journal:  Biophys J       Date:  2016-01-19       Impact factor: 4.033

3.  Structural basis for the gating mechanism of the type 2 ryanodine receptor RyR2.

Authors:  Wei Peng; Huaizong Shen; Jianping Wu; Wenting Guo; Xiaojing Pan; Ruiwu Wang; S R Wayne Chen; Nieng Yan
Journal:  Science       Date:  2016-09-22       Impact factor: 47.728

Review 4.  Mechanisms of ventricular arrhythmias: from molecular fluctuations to electrical turbulence.

Authors:  Zhilin Qu; James N Weiss
Journal:  Annu Rev Physiol       Date:  2014-10-17       Impact factor: 19.318

Review 5.  Multi-scale modeling in biology: how to bridge the gaps between scales?

Authors:  Zhilin Qu; Alan Garfinkel; James N Weiss; Melissa Nivala
Journal:  Prog Biophys Mol Biol       Date:  2011-06-23       Impact factor: 3.667

Review 6.  Dynamic local changes in sarcoplasmic reticulum calcium: physiological and pathophysiological roles.

Authors:  Eric A Sobie; W J Lederer
Journal:  J Mol Cell Cardiol       Date:  2011-07-13       Impact factor: 5.000

7.  Termination of calcium puffs and coupled closings of inositol trisphosphate receptor channels.

Authors:  Steven M Wiltgen; George D Dickinson; Divya Swaminathan; Ian Parker
Journal:  Cell Calcium       Date:  2014-06-26       Impact factor: 6.817

8.  Termination of calcium-induced calcium release by induction decay: an emergent property of stochastic channel gating and molecular scale architecture.

Authors:  D R Laver; C H T Kong; M S Imtiaz; M B Cannell
Journal:  J Mol Cell Cardiol       Date:  2012-11-01       Impact factor: 5.000

Review 9.  Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum.

Authors:  A Fabiato
Journal:  Am J Physiol       Date:  1983-07

10.  Analysis of ryanodine receptor clusters in rat and human cardiac myocytes.

Authors:  Christian Soeller; David Crossman; Ray Gilbert; Mark B Cannell
Journal:  Proc Natl Acad Sci U S A       Date:  2007-09-11       Impact factor: 11.205

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  7 in total

Review 1.  New Insights in Cardiac Calcium Handling and Excitation-Contraction Coupling.

Authors:  Jessica Gambardella; Bruno Trimarco; Guido Iaccarino; Gaetano Santulli
Journal:  Adv Exp Med Biol       Date:  2018       Impact factor: 2.622

2.  Mechanisms of Calcium Leak from Cardiac Sarcoplasmic Reticulum Revealed by Statistical Mechanics.

Authors:  Anna V Maltsev; Michael D Stern; Victor A Maltsev
Journal:  Biophys J       Date:  2019-05-03       Impact factor: 4.033

3.  Disorder in Ca2+ release unit locations confers robustness but cuts flexibility of heart pacemaking.

Authors:  Anna V Maltsev; Michael D Stern; Victor A Maltsev
Journal:  J Gen Physiol       Date:  2022-08-09       Impact factor: 4.000

4.  Functional Heterogeneity of Cell Populations Increases Robustness of Pacemaker Function in a Numerical Model of the Sinoatrial Node Tissue.

Authors:  Alexander V Maltsev; Michael D Stern; Edward G Lakatta; Victor A Maltsev
Journal:  Front Physiol       Date:  2022-04-27       Impact factor: 4.755

5.  Recruiting RyRs to Open in a Ca2+ Release Unit: Single-RyR Gating Properties Make RyR Group Dynamics.

Authors:  Dirk Gillespie
Journal:  Biophys J       Date:  2019-11-23       Impact factor: 4.033

6.  Simulating cardiac Ca2+ release units: effects of RyR cluster size and Ca2+ buffers on diastolic Ca2+ leak.

Authors:  Michael Fill; Dirk Gillespie
Journal:  Pflugers Arch       Date:  2021-02-20       Impact factor: 3.657

Review 7.  Progress in Mathematical Modeling of Gastrointestinal Slow Wave Abnormalities.

Authors:  Peng Du; Stefan Calder; Timothy R Angeli; Shameer Sathar; Niranchan Paskaranandavadivel; Gregory O'Grady; Leo K Cheng
Journal:  Front Physiol       Date:  2018-01-15       Impact factor: 4.566

  7 in total

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