×

Biologically sound formal model of Hsp70 heat induction. (English) Zbl 1416.92059

Summary: A proper response to rapid environmental changes is essential for cell survival and requires effifications in the pattern of gene expression. In this respect, a prominent example is Hsp70, a chaperone protein whose synthesis is dynamically regulated in stress conditions. In this paper, we expand a formal model of Hsp70 heat induction originally proposed in previous articles. To accurately capture various modes of heat shock effects, we not only introduce temperature dependencies in transcription to Hsp70 mRNA and in dissociation of transcriptional complexes, but we also derive a new formal expression for the temperature dependence in protein denaturation. We calibrate our model using comprehensive sets of both previously published experimental data and also biologically justified constraints. Interestingly, we obtain a biologically plausible temperature dependence of the transcriptional complex dissociation, despite the lack of biological constraints imposed in the calibration process. Finally, based on a sensitivity analysis of the model carried out in both deterministic and stochastic settings, we suggest that the regulation of the binding of transcriptional complexes plays a key role in Hsp70 induction upon heat shock. In conclusion, we provide a model that is able to capture the essential dynamics of the Hsp70 heat induction whilst being biologically sound in terms of temperature dependencies, description of protein denaturation and imposed calibration constraints.

MSC:

92C40 Biochemistry, molecular biology
92C42 Systems biology, networks

Software:

SUNDIALS; MOCCASIN
PDFBibTeX XMLCite
Full Text: DOI

References:

[1] Abravaya, K.; Phillips, B.; Morimoto, R. I., Attenuation of the heat response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures, Genes Dev., 5, 11, 2117-2127 (1991)
[2] Abravaya, K.; Phillips, B.; Morimoto, R. I., Heat shock-induced interactions of heat shock transcription factor and the human hsp70 promoter examined by in vivo footprinting, Mol. Cell. Biol., 11, 1, 586-592 (1991)
[3] Ahn, S.-G.; Kim, S.-A.; Yoon, J.-H.; Vacratsis, P., Heat-shock cognate 70 is required for the activation of heat-shock factor 1 in mammalian cells, Biochem. J., 392, 1, 145-152 (2005)
[4] Andrews, G. K.; Harding, M. A.; Calvet, J. P.; Adamson, E. D., The heat shock response in HeLa cells is accompanied by elevated expression of the c-fos proto-oncogene, Mol. Cell. Biol., 7, 10, 3452-3458 (1987)
[5] Baler, R.; Zou, J.; Voellmy, R., Evidence for a role of Hsp70 in the regulation of the heat shock response in mammalian cells, Cell Stress Chaperones, 1, 1, 33-39 (1996)
[6] Banecki, B.; Żylicz, M.; Bertoli, E.; Tanfani, F., Structural and functional relationships in DnaK and DnaK756 heat-shock proteins from escherichia coli, J. Biol. Chem., 267, 35, 25051-25058 (1992)
[7] Brocchieri, L.; Conway de Macario, E.; Macario, A. J.L., Hsp70 genes in the human genome: conservation and differentiation patterns predict a wide array of overlapping and specialized functions, BMC Evol. Biol., 8, 19 (2008)
[8] Brunet Simioni, M.; De Thonel, A.; Hammann, A.; Joly, A.-L.; Bossis, G.; Fourmaux, E.; Bouchot, A.; Landry, J.; Piechaczyk, M.; Garrido, C., Heat shock protein 27 is involved in SUMO-2/3 modification of heat shock factor 1 and thereby modulates the transcription factor activity, Oncogene, 28, 37, 3332-3344 (2009)
[9] Chaudhuri, T. K.; Paul, S., Protein-misfolding diseases and chaperone-based therapeutic approaches, FEBS J., 273, 1331-1349 (2006)
[10] Chelliah, V.; Juty, N.; Ajmera, I.; Ali, R.; Dumousseau, M.; Glont, M.; Hucka, M.; Jalowicki, G.; Keating, S.; Knight-Schrijver, V.; Lloret-Villas, A.; Nath Natarajan, K.; Pettit, J.-B.; Rodriguez, N.; Schubert, M.; Wimalaratne, S. M.; Zhao, Y.; Hermjakob, H.; Le Novère, N.; Laibe, C., Biomodels: ten-year anniversary, Nucl. Acids Res., 43, D1, D542-D548 (2015)
[11] Chu, K. F.; Dupuy, D. E., Thermal ablation of tumours: biological mechanisms and advances in therapy, Nat. Rev. Cancer, 14, 3, 199-208 (2014)
[12] Dworniczak, B.; Mirault, M.-E., Structure and expression of a human gene coding for a 71 kd heat shock ’cognate’ protein, Nucleic Acids Res., 15, 13, 5181-5197 (1987)
[13] Finka, A.; Goloubinoff, P., Proteomic data from human cell cultures refine mechanisms of chaperone-mediated protein homeostasis, Cell Stress Chaperones, 18, 5, 591-605 (2013)
[14] Fortugno, P.; Beltrami, E.; Plescia, J.; Fontana, J.; Pradhan, D.; Marchisio, P. C.; Sessa, W. C.; Altieri, D. C., Regulation of survivin function by Hsp90, Proc. Natl. Acad. Sci. U.S.A., 100, 24, 13791-13796 (2003)
[15] Fujimoto, M., Transcriptional regulation by HSF, (Nakai, A., Heat Shock Factor (2016), Springer Japan: Springer Japan Tokyo), 73-89
[16] Fujimoto, M.; Takaki, E.; Takii, R.; Tan, K.; Prakasam, R.; Hayashida, N.; Iemura, S.; Natsume, T.; Nakai, A., RPA assists HSF1 access to nucleosomal DNA by recruiting histone chaperone FACT, Mol. Cell, 48, 2, 182-194 (2012)
[17] Garnier, C.; Protasevich, I.; Gilli, R.; Tsvetkov, P.; Lobachov, V.; Peyrot, V.; Briand, C.; Makarov, A., The two-stage process of the heat shock protein 90 thermal denaturation: effect of calcium and magnesium, Biochem. Biophys. Res. Commun., 249, 1, 197-201 (1998)
[18] Gómez, H. F.; Hucka, M.; Keating, S. M.; Nudelman, G.; Iber, D.; Sealfon, S. C., MOCCASIN: Converting MATLAB ODE models to SBML, Bioinformatics, 32, 12, 1905-1906 (2016)
[19] Hageman, J.; van Waarde, M. A.W. H.; Zylicz, A.; Walerych, D.; Kampinga, H. H., The diverse members of the mammalian HSP70 machine show distinct chaperone-like activities, Biochem. J., 435, 1, 127-142 (2011)
[20] Herbomel, G.; Kloster-Landsberg, M.; Folco, E. G.; Col, E.; Usson, Y.; Vourc’h, C.; Delon, A.; Souchier, C., Dynamics of the full length and mutated heat shock factor 1 in human cells, PLoS One, 8, 7, e67566 (2013)
[21] Hildebrandt, B.; Wust, P.; Ahlers, O.; Dieing, A.; Sreenivasa, G.; Kerner, T.; Felix, R.; Riess, H., The cellular and molecular basis of hyperthermia, Crit. Rev. Oncol. Hematol., 43, 1, 33-56 (2002)
[22] Hindmarsh, A. C.; Brown, P. N.; Grant, K. E.; Lee, S. L.; Serban, R.; Shumaker, D. E.; Woodward, C. S., SUNDIALS: suite of nonlinear and differential/algebraic equation solvers, ACM Trans. Math. Softw., 31, 3, 363-396 (2005) · Zbl 1136.65329
[23] Jetka, T.; Charzyńska, A.; Gambin, A.; Stumpf, M. P.; Komorowski, M., StochDecomp-Matlab package for noise decomposition in stochastic biochemical systems, Bioinform., 30, 1, 137-138 (2014)
[24] van Kampen, N. G., Stochastic Processes in Physics and Chemistry (2007), Elsevier: Elsevier Amsterdam · Zbl 0974.60020
[25] Kline, M. P.; Morimoto, R. I., Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation, Mol. Cell. Biol., 17, 4, 2107-2115 (1997)
[26] Kloster-Landsberg, M.; Herbomel, G.; Wang, I.; Derouard, J.; Vourc’h, C.; Usson, Y.; Souchier, C.; Delon, A., Cellular response to heat shock studied by multiconfocal fluorescence correlation spectroscopy, Biophys. J., 103, 6, 1110-1119 (2012)
[27] Komorowski, M.; Miękisz, J.; Stumpf, M. P.H., Decomposing noise in biochemical signaling systems highlights the role of protein degradation, Biophys. J., 104, 8, 1783-1793 (2013)
[28] Kroeger, P. E.; Sarge, K. D.; Morimoto, R. I., Mouse heat shock transcription factors 1 and 2 prefer a trimeric binding site but interact differently with the HSP70 heat shock element, Mol. Cell. Biol., 13, 6, 3370-3383 (1993)
[29] Lanneau, D.; Wettstein, G.; Bonniaud, P.; Garrido, C., Heat shock proteins: cell protection through protein triage, Sci. World J., 10, 1543-1552 (2010)
[30] Lepock, J. R.; Frey, H. E.; Ritchie, K. P., Protein denaturation in intact hepatocytes and isolated cellular organelles during heat shock, J. Cell Biol., 122, 6, 1267-1276 (1993)
[31] Lepock, J. R.; Frey, H. E.; Rodahl, A. M.; Kruuv, J., Thermal analysis of CHL V79 cells using differential scanning calorimetry: implications for hyperthermic cell killing and the heat shock response, J. Cellular Physiol., 137, 1, 14-24 (1988)
[32] Lodish, H. F.; Jacobsen, M., Regulation of hemoglobin synthesis. Equal rates of translation and termination of \(α\)- and \(β\)-globin chains., J. Biol. Chem., 247, 11, 3622-3629 (1972)
[33] Loos, C.; Krause, S.; Hasenauer, J., Hierarchical optimization for the efficient parametrization of ODE models, Bioinformatics, 34, 24, 4266-4273 (2018)
[34] Mayer, M. P.; Bukau, B., Hsp70 chaperones: cellular functions and molecular mechanism, Cell Mol Life Sci., 62, 6, 670-684 (2005)
[35] Mayer, M. P.; Schröder, H.; Rödiger, S.; Paal, K.; Laufen, T.; Bukau, B., Multistep mechanism of substrate binding determines chaperone activity of Hsp70, Nat Struct Biol., 7, 7, 586-593 (2000)
[36] Miguel, A.; Monton, F.; Li, T.; Gomez-Herreros, F.; Chavez, S.; Alepuz, P.; Perez-Ortin, J. E., External conditions inversely change the RNA polymerase II elongation rate and density in yeast, Biochim. Biophys. Acta, 1829, 11, 1248-1255 (2013)
[37] Mizera, A.; Gambin, B., Stochastic modelling of the eukaryotic heat shock response, J. Theor. Biol., 265, 3, 455-466 (2010) · Zbl 1461.92024
[38] Moran, U.; Phillips, R.; Milo, R., Snapshot: key numbers in biology, Cell, 141, 1262-1262.e1 (2010)
[39] Morimoto, R. I., Cells in stress: transcriptional activation of heat shock genes, Science, 259, 5100, 1409-1410 (1993)
[40] Mosser, D. D.; Theodorakis, N. G.; Morimoto, R. I., Coordinate changes in heat shock element-binding activity and HSP70 gene transcription rates in human cells, Mol. Cell. Biol., 8, 11, 4736-4744 (1988)
[41] Nakai, A., Molecular basis of HSF regulation, Nat. Struct. Mol. Biol., 23, 2, 93-95 (2016)
[42] Nunes, S. L.; Calderwood, S. K., Heat shock factor-1 and the heat shock cognate 70 protein associate in high molecular weight complexes in the cytoplasm of NIH-3T3 cells, Bioch. Biophys. Res. Commun., 213, 1, 1-6 (1995)
[43] O’Brien, T.; Lis, J. T., Rapid changes in drosophila transcription after an instantaneous heat shock, Mol. Cell. Biol., 13, 6, 3456-3463 (1993)
[44] Palleros, D. R.; Welch, W. J.; Fink, A. L., Interaction of hsp70 with unfolded proteins: effects of temperature and nucleotides on the kinetics of binding, Proc. Natl. Acad. Sci. U.S.A., 88, 13, 5719-5723 (1991)
[45] Peper, A.; Grimbergen, C. A.; Spaan, J. A.E.; Souren, J. E.M.; van Wijk, R., A mathematical model of the hsp70 regulation in the cell, Int. J. Hyperth., 14, 1, 97-124 (1998)
[46] Petersen, R. B.; Lindquist, S., Regulation of HSP70 synthesis by messenger RNA degradation, Cell Regul., 1, 1, 135-149 (1989)
[47] Petre, I.; Mizera, A.; Hyder, C. L.; Meinander, A.; Mikhailov, A.; Morimoto, R. I.; Sistonen, L.; Eriksson, J. E.; Back, R.-J., A simple mass-action model for the eukaryotic heat shock response and its mathematical validation, Nat Comput., 10, 1, 595-612 (2011)
[48] Petre, I.; Mizera, A.; Hyder, C. L.; Mikhailov, A.; Eriksson, J. E.; Sistonen, L.; Back, R.-J., A new mathematical model for the heat shock response, (Condon, A.; Harel, D.; Kok, J. N.; Salomaa, A.; Winfree, E., Algorithmic Bioprocesses (2009), Springer Berlin Heidelberg: Springer Berlin Heidelberg Berlin, Heidelberg), 411-425
[49] Proctor, C. J.; Lorimer, I. A.J., Modelling the role of the Hsp70/Hsp90 system in the maintenance of protein homeostasis, PLoS ONE, 6, e22038 (2011)
[50] Qian, S.-B.; McDonough, H.; Boellmann, F.; Cyr, D. M.; Patterson, C., CHIP-Mediated stress recovery by sequential ubiquitination of substrates and Hsp70, Nature, 440, 7083, 551-555 (2006)
[51] Qin, X.; Ahn, S.; Speed, T. P.; Rubin, G. M., Global analyses of mRNA translational control during early drosophila embryogenesis, Genome Biol., 8, 4, R63 (2007)
[52] Rice, G. A.; Chamberlin, M. J.; Kane, C. M., Contacts between mammalian RNA polymerase II and the template DNA in a ternary elongation complex, Nucleic Acids Res., 21, 1, 113-118 (1993)
[53] Rieger, T. R.; Morimoto, R. I.; Hatzimanikatis, V., Mathematical modeling of the eukaryotic heat-shock response: dynamics of the hsp70 promoter, Biophys. J., 88, 3, 1646-1658 (2005)
[54] Rybiński, M.; Szymańska, Z.; Lasota, S.; Gambin, A., Modelling the efficacy of hyperthermia treatment, J. Royal Soc. Interface, 10, 88 (2013)
[55] Sarge, K. D.; Murphy, S. P.; Morimoto, R. I., Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress, Mol. Cell. Biol., 13, 3, 1392-1407 (1993)
[56] Scheff, J. D.; Stallings, J. D.; Reifman, J.; Rakesh, V., Mathematical modeling of the heat-shock response in HeLa cells, Biophys. J., 109, 2, 182-193 (2015)
[57] Schwarz, G., Estimating the dimension of a model, Ann. Stat., 6, 2, 461-464 (1978) · Zbl 0379.62005
[58] Sehgal, P. B.; Derman, E.; Molloy, G. R.; Tamm, I.; Darnell, J. E., 5,6-dichloro-1-beta-d-ribofuranosylbenzimidazole inhibits initiation of nuclear heterogeneous RNA chains in HeLa cells, Science, 194, 4263, 431-433 (1976)
[59] Shi, Y.; Mosser, D. D.; Morimoto, R. I., Molecular chaperones as HSF1-specific transcriptional repressors, Genes Dev., 12, 5, 654-666 (1998)
[60] Sivéry, A.; Courtade, E.; Thommen, Q., A minimal titration model of the mammalian dynamical heat shock response, Phys. Biol., 13, 6, 066008 (2016)
[61] Skowyra, D.; Georgopoulos, C.; Żylicz, M., The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner, Cell, 62, 5, 939-944 (1990)
[62] Sriram, K.; Rodriguez-Fernandez, M.; Doyle, F. J., A detailed modular analysis of heat-shock protein dynamics under acute and chronic stress and its implication in anxiety disorders, PLOS ONE, 7, 8, 1-15 (2012)
[63] Stege, G. J.J.; Brunsting, J. F.; Kampinga, H. H.; Konings, A. W.T., Thermotolerance and nuclear protein aggregation: protection against initial damage or better recovery?, J. Cell. Physiol., 164, 3, 579-586 (1995)
[64] Stroppolo, M. E.; Falconi, M.; Caccuri, A. M.; Desideri, A., Superefficient enzymes, Cell Mol. Life Sci., 58, 10, 1451-1460 (2001)
[65] Szymańska, Z.; Żylicz, M., Mathematical modeling of heat shock protein synthesis in response to temperature change, J. Theor. Biol., 259, 3, 562-569 (2009) · Zbl 1402.92186
[66] Theodorakis, N. G.; Drujan, D.; De Maio, A., Thermotolerant cells show an attenuated expression of Hsp70 after heat shock, J. Biol. Chem., 274, 17, 12081-12086 (1999)
[67] Theodorakis, N. G.; Morimoto, R. I., Posttranscriptional regulation of hsp70 expression in human cells: effects of heat shock, inhibition of protein synthesis, and adenovirus infection on translation and mRNA stability, Mol. Cell. Biol., 7, 12, 4357-4368 (1987)
[68] Turányi, T., Sensitivity analysis of complex kinetic systems. Tools and applications, J. Math. Chem., 5, 3, 203-248 (1990)
[69] Weber, P.; Hasenauer, J.; Allgöwer, F.; Radde, N., Parameter estimation and identifiability of biological networks using relative data, IFAC Proc. Vol., 44, 1, 11648-11653 (2011) · Zbl 1280.39011
[70] Wickner, S.; Maurizi, M. R.; Gottesman, S., Posttranslational quality control: folding, refolding, and degrading proteins, Science, 286, 5446, 1888-1893 (1999)
[71] Zhao, L.; Kroenke, C. D.; Song, J.; Piwnica-Worms, D.; Ackerman, J. J.H.; Neil, J. J., Intracellular water-specific MR of microbead-adherent cells: the HeLa cell intracellular water exchange lifetime, NMR Biomed., 21, 2, 159-164 (2008)
[72] Zou, J.; Guo, Y.; Guettouche, T.; Smith, D. F.; Voellmy, R., Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1, Cell, 94, 4, 471-480 (1998)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.