Nuclear Pores Enable Sustained Perinuclear Calcium Oscillations

Overview

Journal BMC Syst Biol

Publisher Biomed Central

Specialty Biology

Date 2016 Jul 25

PMID 27449670

Citations 7

Authors

Teresa Vaz Martins

Matthew J Evans

Derin B Wysham

Richard J Morris

Affiliations

Soon will be listed here.

Abstract

Background: Calcium signalling relies on the flux of calcium ions across membranes yet how signals in different compartments are related remains unclear. In particular, similar calcium signals on both sides of the nuclear envelope have been reported and attributed to passive diffusion through nuclear pores. However, observed differing cytosolic and nucleosolic calcium signatures suggest that the signalling machinery in these compartments can act independently.

Results: We adapt the fire-diffuse-fire model to investigate the generation of perinuclear calcium oscillations. We demonstrate that autonomous spatio-temporal calcium patterns are still possible in the presence of nuclear and cytosolic coupling via nuclear pores. The presence or absence of this autonomy is dependent upon the strength of the coupling and the maximum firing rate of an individual calcium channel. In all cases, coupling through the nuclear pores enables robust signalling with respect to changes in the diffusion constant.

Conclusions: We show that contradictory interpretations of experimental data with respect to the autonomy of nuclear calcium oscillations can be reconciled within one model, with different observations being a consequence of varying nuclear pore permeabilities for calcium and refractory conditions of channels. Furthermore, our results provide an explanation for why calcium oscillations on both sides of the nuclear envelope may be beneficial for sustained perinuclear signaling.

Citing Articles

Nuclear Calcium in Cardiac (Patho)Physiology: Small Compartment, Big Impact.

Kiessling M, Djalinac N, Voglhuber J, Ljubojevic-Holzer S Biomedicines. 2023; 11(3).

PMID: 36979939 PMC: 10046765. DOI: 10.3390/biomedicines11030960.

Encoding, transmission, decoding, and specificity of calcium signals in plants.

Allan C, Morris R, Meisrimler C J Exp Bot. 2022; 73(11):3372-3385.

PMID: 35298633 PMC: 9162177. DOI: 10.1093/jxb/erac105.

An update on passive transport in and out of plant cells.

Tomkins M, Hughes A, Morris R Plant Physiol. 2022; 187(4):1973-1984.

PMID: 35235675 PMC: 8644452. DOI: 10.1093/plphys/kiab406.

Functional Consequences of Calcium-Dependent Synapse-to-Nucleus Communication: Focus on Transcription-Dependent Metabolic Plasticity.

Hagenston A, Bading H, Bas-Orth C Cold Spring Harb Perspect Biol. 2019; 12(4).

PMID: 31570333 PMC: 7111253. DOI: 10.1101/cshperspect.a035287.

What Drives Symbiotic Calcium Signalling in Legumes? Insights and Challenges of Imaging.

Vaz Martins T, Livina V Int J Mol Sci. 2019; 20(9).

PMID: 31067698 PMC: 6539980. DOI: 10.3390/ijms20092245.

References

Hardingham G, Chawla S, Johnson C, Bading H . Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature. 1997; 385(6613):260-5. DOI: 10.1038/385260a0. View

Casey A, Wente S . Nuclear transport: shifting gears in fungal nuclear and cytoplasmic organization. Curr Biol. 2012; 22(19):R846-8. DOI: 10.1016/j.cub.2012.08.043. View

Winey M, Yarar D, Giddings Jr T, Mastronarde D . Nuclear pore complex number and distribution throughout the Saccharomyces cerevisiae cell cycle by three-dimensional reconstruction from electron micrographs of nuclear envelopes. Mol Biol Cell. 1997; 8(11):2119-32. PMC: 25696. DOI: 10.1091/mbc.8.11.2119. View

Queisser G, Wiegert S, Bading H . Structural dynamics of the cell nucleus: basis for morphology modulation of nuclear calcium signaling and gene transcription. Nucleus. 2011; 2(2):98-104. PMC: 3127091. DOI: 10.4161/nucl.2.2.15116. View

Kinoshita Y, Kalir T, Dottino P, Kohtz D . Nuclear distributions of NUP62 and NUP214 suggest architectural diversity and spatial patterning among nuclear pore complexes. PLoS One. 2012; 7(4):e36137. PMC: 3338603. DOI: 10.1371/journal.pone.0036137. View

Xiong T, Bourque S, Lecourieux D, Amelot N, Grat S, Briere C . Calcium signaling in plant cell organelles delimited by a double membrane. Biochim Biophys Acta. 2006; 1763(11):1209-15. DOI: 10.1016/j.bbamcr.2006.09.024. View

Dolmetsch R, Xu K, Lewis R . Calcium oscillations increase the efficiency and specificity of gene expression. Nature. 1998; 392(6679):933-6. DOI: 10.1038/31960. View

Erickson E, Mooren O, Moore D, Krogmeier J, Dunn R . The role of nuclear envelope calcium in modifying nuclear pore complex structure. Can J Physiol Pharmacol. 2006; 84(3-4):309-18. DOI: 10.1139/y05-109. View

Imamoto N, Funakoshi T . Nuclear pore dynamics during the cell cycle. Curr Opin Cell Biol. 2012; 24(4):453-9. DOI: 10.1016/j.ceb.2012.06.004. View

10.

Danker T, Schillers H, STORCK J, Shahin V, Kramer B, Wilhelmi M . Nuclear hourglass technique: an approach that detects electrically open nuclear pores in Xenopus laevis oocyte. Proc Natl Acad Sci U S A. 1999; 96(23):13530-5. PMC: 23982. DOI: 10.1073/pnas.96.23.13530. View

11.

Fricker M, Runions J, Moore I . Quantitative fluorescence microscopy: from art to science. Annu Rev Plant Biol. 2006; 57:79-107. DOI: 10.1146/annurev.arplant.57.032905.105239. View

12.

Eder A, Bading H . Calcium signals can freely cross the nuclear envelope in hippocampal neurons: somatic calcium increases generate nuclear calcium transients. BMC Neurosci. 2007; 8:57. PMC: 1950097. DOI: 10.1186/1471-2202-8-57. View

13.

Santella L . The cell nucleus: an Eldorado to future calcium research?. J Membr Biol. 1996; 153(2):83-92. DOI: 10.1007/s002329900112. View

14.

Hohendanner F, McCulloch A, Blatter L, Michailova A . Calcium and IP3 dynamics in cardiac myocytes: experimental and computational perspectives and approaches. Front Pharmacol. 2014; 5:35. PMC: 3944219. DOI: 10.3389/fphar.2014.00035. View

15.

Genka C, Ishida H, Ichimori K, Hirota Y, Tanaami T, Nakazawa H . Visualization of biphasic Ca2+ diffusion from cytosol to nucleus in contracting adult rat cardiac myocytes with an ultra-fast confocal imaging system. Cell Calcium. 1999; 25(3):199-208. DOI: 10.1054/ceca.1999.0026. View

16.

Mauger J . Role of the nuclear envelope in calcium signalling. Biol Cell. 2011; 104(2):70-83. DOI: 10.1111/boc.201100103. View

17.

Cardenas C, Escobar M, Garcia A, Osorio-Reich M, Hartel S, Foskett J . Visualization of inositol 1,4,5-trisphosphate receptors on the nuclear envelope outer membrane by freeze-drying and rotary shadowing for electron microscopy. J Struct Biol. 2010; 171(3):372-81. PMC: 2916234. DOI: 10.1016/j.jsb.2010.05.003. View

18.

Belgareh N, Doye V . Dynamics of nuclear pore distribution in nucleoporin mutant yeast cells. J Cell Biol. 1997; 136(4):747-59. PMC: 2132498. DOI: 10.1083/jcb.136.4.747. View

19.

Rodrigues M, Gomes D, Nathanson M, Leite M . Nuclear calcium signaling: a cell within a cell. Braz J Med Biol Res. 2008; 42(1):17-20. PMC: 2989390. DOI: 10.1590/s0100-879x2008005000050. View

20.

Maeshima K, Iino H, Hihara S, Imamoto N . Nuclear size, nuclear pore number and cell cycle. Nucleus. 2011; 2(2):113-8. PMC: 3127093. DOI: 10.4161/nucl.2.2.15446. View