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Membrane associated complexes : new approach to calciumdynamics modelling

Published online by Cambridge University Press:  20 December 2012

M. Dyzma ,
P. Szopa  and
B. Kaźmierczak
M. Dyzma
Affiliation:
Institute of Fundamental Technological Research, Polish Academy of Sciences, Warsaw
P. Szopa
Affiliation:
Institute of Fundamental Technological Research, Polish Academy of Sciences, Warsaw Faculty of Mathematics, Informatics and Mechanics, University of Warsaw
B. Kaźmierczak*
Affiliation:
Institute of Fundamental Technological Research, Polish Academy of Sciences, Warsaw
*
⋆ Corresponding author. E-mail: [email protected]
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Abstract

Mitochondria are one of the most important organelles determining Ca2+regulatory pathway in the cell. Recent experiments suggested the existence of cytosolicmicrodomains with locally elevated calcium concentration (CMDs) in the nearest vicinity ofthe outer mitochondrial membrane (OMM). These intermediate physical connections betweenendoplasmic reticulum (ER) and mitochodria are called MAM (mitochondria-associated ERmembrane) complexes.

The aim of this paper is to take into account the direct calcium flowfrom ER to mitochondria implied by the existence of MAMs and perform detailed numericalanalysis of the influence of this flow on the type and shape of calcium oscillations.Depending on the permeability of MAMs interface and ER channels, different patterns ofoscillations appear (simple, bursting and chaotic). For some parameters the oscillatorypattern disappear and the system tends to a steady state with extremely high calcium levelin mitochondria, which can be interpreted as a crucial point at the beginning of anapoptotic pathway.

Keywords

Ca2+ signalingmitochodrial Ca2+ transportMAMsthree pool modelbistabilityapoptosis
Type
Research Article
Information
Mathematical Modelling of Natural Phenomena , Volume 7 , Issue 6: Biological oscillations , 2012 , pp. 167 - 186
Copyright
© EDP Sciences, 2012

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References

Références

Clapham, D.E.. Calcium signaling. Cell, 131 (2007), 1047–1058. CrossRefGoogle ScholarPubMed
Laude, A.J., Simpson, A.W.M.. Compartmentalized signalling : Ca2+ compartments, microdomains and the many facets of Ca2+ signalling. FEBS J., 276 (2009), 1800–1816. CrossRefGoogle ScholarPubMed
Montell, C.. The latest waves in calcium signaling. Cell, 122 (2005), 157–163. CrossRefGoogle ScholarPubMed
Oster, A.M., Thomas, B., Terman, D., Fall, C.P.. The low conductance mitochondrial permeability transition pore confers excitability and CICR wave propagation in a computational model. J Theor Biol, 273 (2011), 216–231. CrossRefGoogle Scholar
Hajnóczky, G., Csordás, G., Madesh, M., Pacher, P.. The machinery of local Ca2+ signalling between sarco-endoplasmic reticulum and mitochondria. J. Physiology, 529 (2000), 69–81. CrossRefGoogle ScholarPubMed
Chipuk, J.E., Bouchier-Hayes, L., Green, D.R.. Mitochondrial outer membrane permeabilization during apoptosis : the innocent bystander scenario. Cell Death Differ., 13 (2006) 1396–1400. CrossRefGoogle ScholarPubMed
Tait, S.W., Parsons, M.J., Llambi, F., Bouchier-Hayes, L., Connell, S., Munoz-Pinedo, C., Green, D.R.. Resistance to caspase-independent cell death requires persistence of intact mitochondria. Dev. Cell, 18 (2010) 802-81. CrossRefGoogle ScholarPubMed
Hajnóczky, G., Csordás, G., Das, S., Garcia-Perez, C., Saotome, M., Roy, S.S., Yi, M.. Mitochondrial calcium signalling and cell death : approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis. Cell Calcium, 40 (2006) 553–560. CrossRefGoogle ScholarPubMed
Borghans, J.A.M., Dupont, G., Goldbeter, A.. Complex intracellular calcium oscillations. A theoretical exploration of possible mechanisms. Biophysical Chemistry, 66 (1997) 25–41. CrossRefGoogle ScholarPubMed
Marhl, M., Haberichter, T., Brumen, M., Heinrich, R.. Complex calcium oscillations and the role of mitochondria and cytosolic proteins. Biosystems, 57 (2000) 75–86. CrossRefGoogle ScholarPubMed
Csordás, G., Várnai, P., Golenár, T., Roy, S., Purkins, G., Schneider, T.G., Balla, T., Hajnóczky, G.. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell, 39 (2010) 121–132. CrossRefGoogle Scholar
Dennis, E.A., Kennedy, E.P.. Intracellular sites of lipid synthesis and the biogenesis of mitochondria. J Lipid Res, 13 (1972) 263–267. Google ScholarPubMed
Rusinol, A.E., Cui, Z., Chen, M.H., Vance, J.E.. A unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins. J Biol Chem, 269 (1994) 27494–27502. Google Scholar
Giorgi, C., De Stefani, D., Bononi, A., Rizzuto, R., Pinton, P.. Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int J Biochem Cell Biol, 41 (2009) 1817–1827. CrossRefGoogle ScholarPubMed
Lebiedzinska, M., Szabadkai, G., Jones, A.W.E., Duszynski, J., Wieckowski, M.R.. Interactions between the endoplasmic reticulum, mitochondria, plasma membrane and other subcellular organelles. Int J Biochem Cell Biol, 41 (2009) 1805–1816. CrossRefGoogle ScholarPubMed
Giacomello, M., Drago, I., Bortolozzi, M., Scorzeto, M., Gianelle, A., Pizzo, P., Pozzan, T.. Ca2+ hot spots on the mitochondrial surface are generated by Ca2+ mobilization from stores, but not by activation of store-operated Ca2+ channels. Mol Cell., 38(2) (2010) 280–290. CrossRefGoogle Scholar
Csordás, G., Renken, C., Várnai, P., Walter, L., Weaver, D., Buttle, K.F., Balla, T., Mannella, C.A., Hajnóczky, G.. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol, 174 (2006) 915–921. CrossRefGoogle Scholar
Hayashi, T., Rizzuto, R., Hajnóczky, G., Su, T.-P.. MAM : more than just a housekeeper. Trends Cell Biol, 19 (2009) 81–88. CrossRefGoogle ScholarPubMed
Schuster, S., Marhl, M., Höfer, T.. Modelling of simple and complex calcium oscillations. From single-cell responses to intercellular signalling. Eur J Biochem, 269 (2002) 1333–1355. CrossRefGoogle ScholarPubMed
D. Hariprasad, M. McNulty, J. Shi, P. Tian. Three-pool model of calcium signaling. https://digitalarchive.wm.edu/bitstream/handle/10288/1179/Hariprasad%20Daniel%202009.pdf?sequence=1 (2009).
Marhl, M., Schuster, S., Brumen, M.. Mitochondria as an important factor in the maintenance of constant amplitudes of cytosolic calcium oscillations. Biophysical Chemistry, 71 (1998) 125–132. CrossRefGoogle Scholar
H. Coe, M. Michalak. Calcium binding chaperones of the endoplasmic reticulum. Gen Physiol Biophys, 28 Spec No Focus (2009) F96–F103.
B. Schwaller. Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol, 2(11) a004051.
Parekh, A.B.. Mitochondrial regulation of intracellular Ca2+ signaling : more than just simple Ca2+ buffers. News Physiol Sci, 18 (2003) 252–256. Google Scholar
J. Keener, J. Sneyd. Mathematical Physiology, Springer, New York, 1998.
Sneyd, J., Duffy, A., Dale, P.D.. Traveling Waves in Buffered Systems : Applications to Calcium Waves. SIAM J. Appl. Math., 58 (1998) 1178–1192. Google Scholar
Skupin, A., Falcke, M.. From puffs to global Ca2+ signals : how molecular properties shape global signals. Chaos, 19 (2009) 037111. CrossRefGoogle Scholar
Hoogenboom, B.W., Suda, K., Engel, A., Fotiadis, D.. The supramolecular assemblies of voltage-dependent anion channels in the native membrane. J Mol Biol., 370 (2007) 246–255. CrossRefGoogle ScholarPubMed
Shoshan-Barmatz, V., De Pinto, V., Zweckstetter, M., Raviv, Z., Keinan, N., Arbel, N.. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med., 31 (2010) 227–285. CrossRefGoogle Scholar
Dupont, G., Combettes, L.. What can we learn from the irregularity of Ca2+ oscillations ?. Chaos, 19 (2009) 037112. CrossRefGoogle ScholarPubMed
Wagner, J., Keizer, J.. Effects of rapid buffers on Ca2+ diffusion and Ca2+ oscillations. Biophys J., 67 (1994) 447–456. CrossRefGoogle Scholar
Dawson, A.P., Rich, G.T., Loomis-Husselbee, J.W.. Estimation of the free [Ca2+] gradient across endoplasmic reticulum membranes by a null-point method. Biochem J., 310 (1995) 371–374. CrossRefGoogle Scholar
Hoth, M., Fanger, C.M., Lewis, R.S.. Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J Cell Biol., 137 (1997) 633–648. CrossRefGoogle ScholarPubMed
Li, Y.-X., Keizer, J., Stojilkovic, S.S., Rinzel, J.. Calcium excitability of the ER membrane : an explanation for IP3-induced Ca2+ oscillations. Am J Physiol Cell Physiol, 269 (1995) C1079–C1092. Google ScholarPubMed
Sneyd, J., Tsaneva-Atanasova, K., Yule, D. I., Thompson, J. L., Shuttleworth, T. J.. Control of calcium oscillations by membrane fluxes. Proc Natl Acad Sci USA, 101 (2004) 1392–1396. CrossRefGoogle ScholarPubMed
Babcock, D.F., Hille, B.. Mitochondrial oversight of cellular Ca2+ signaling. Curr. Opin. Neurobiol., 8 (1998) 398–404. CrossRefGoogle ScholarPubMed
Falcke, M.. Reading the patterns in living cells - the physics of Ca2+ signaling. Advances in Physics, 53 (2004) 255–440. CrossRefGoogle Scholar
Rasola, A., Bernardi, P.. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis, 12 (2007) 815–833. CrossRefGoogle ScholarPubMed
Babcock, D.F., Herrington, J., Goodwin, P.C., Park, Y.B., Hille, B.. Mitochondrial participation in the intracellular Ca2+ network. J. Cell Biol, 136 (1997) 833–844. CrossRefGoogle ScholarPubMed
Hehl, S., Golard, A., Hille, B.. Involvement of mitochondria in intracellular calcium sequestration by rat gonadotropes. Cell Calcium, 20 (1996) 515–524. CrossRefGoogle ScholarPubMed
Svichar, N., Shishkin, V., Kostyuk, P.. Mitochondrial participation in modulation of calcium transients in DRG neurons. Neuroreport, 10 (1999) 1257–1261. CrossRefGoogle Scholar
V.V. Chepyzhov, M.I. Vishik. Attractors for Equations of Mathematical Physics. American Mathematical Society, Providence RI, 2002.
W. Govaerts, Yu.A. Kuznetsov, http://www.matcont.ugent.be.
Joseph, S.K., Hajnóczky, G.. IP3 receptors in cell survival and apoptosis : Ca2+ release and beyond. Apoptosis, 12 (2007) 951–968. CrossRefGoogle ScholarPubMed
Roy, S.S., Hajnóczky, G.. Calcium, mitochondria and apoptosis studied by fluorescence measurements. Methods, 46 (2008) 213–223. CrossRefGoogle ScholarPubMed
Rizzuto, R., Pinton, P., Ferrari, D., Chami, M., Szabadkai, G., Magalhães, P.J., Di Virgilio, F., Pozzan, T.. Calcium and apoptosis : facts and hypotheses. Oncogene, 22 (2003) 8619–8627. CrossRefGoogle ScholarPubMed
V.N. Govorukhin. http://www.math.rsu.ru/mexmat/kvm/matds/.
R. Hegger, H. Kantz, T. Schreiber. http://www.mpipks-dresden.mpg.de/~tisean/Tisean_3.0.1/index.html.
H. Kantz, T. Schreiber. Nonlinear Time Series Analysis, Cambridge University Press, Cambridge, 2004.
Özer, A.B., Akin, E.. Tools for detecting chaos. SAU Fen Bilimleri Enstitusu Dergisi, 9 (2005) 60–66. Google Scholar
Park, B.J., Lee, D.G., Yu, J.R., Jung, S.K., Choi, K., Lee, J., Lee, J., Kim, Y.S., Lee, J.I., Kwon, J.Y., Lee, J., Singson, A., Song, W.K., Eom, S.H., Park, C.S., Kim, D.H., Bandyopadhyay, J., Ahnn, J.. Calreticulin, a calcium-binding molecular chaperone, is required for stress response and fertility in Caenorhabditis elegans. Mol Biol Cell., 12(9) (2001) 2835–2845. CrossRefGoogle ScholarPubMed
Ellgaard, L., Helenius, A.. ER quality control : towards an understanding at the molecular level. Current Opinion in Cell Biology, 13(4) (2001) 431–437. CrossRefGoogle Scholar
Anelli, T., Alessio, M., Mezghrani, A., Simmen, T., Talamo, F., Bachi, A., Sitia, R.. ERp44, a novel endoplasmic reticulum folding assistant of thethioredoxin family. The EMBO Journal, 21 (2002) 835–844. CrossRefGoogle ScholarPubMed
Hayashi, T., Su, T.P.. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell, 131(3) (2007) 596–610. CrossRefGoogle Scholar
Jethmalani, S.M., Henle, K.J.. Calreticulin associates with stress proteins : implications for chaperone function during heat stress. J Cell Biochem., 69(1) (1998) 30–43. 3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Mizzen, L.A., Kabiling, A.N., Welch, W.J.. The two mammalian mitochondrial stress proteins, grp 75 and hsp 58, transiently interact with newly synthesized mitochondrial proteins. Cell Regul., 2(2) (1991) 165–179.Google Scholar