Abstract
We investigated the dissociation of single-ring heptameric GroEL (SR1) by high hydrostatic pressure in the range 0.5–3.0 kbar. The kinetics were studied as a function of temperature in the range 15–35 °C. The dissociation processes at each pressure and temperature showed biphasic behavior. The slower rate (k 1,obs) was confirmed to be the self-dissociation of SR1 at any specific temperature at atmospheric pressure. This dissociation was pressure independent and followed concentration-dependent first-order kinetics. The self-dissociation rates followed normal Eyring plots (ln k 1,obs/T vs. 1/T) from which the free energy of activation (ΔG ≠ = 22 ± 0.3 kcal mol−1), enthalpy of activation (ΔH ≠ = 18 ± 0.5 kcal mol−1), and entropy of activation (ΔS ≠ = −15 ± 1 kcal mol−1) were evaluated. The effect of pressure on the dissociation rates resulted in nonlinear behavior (ln k 2,obs vs. pressure) at all the temperatures studied indicating that the activation volumes were pressure dependent. Activation volumes at zero pressure (V ≠ o) and compressibility factors (β≠) for the dissociation rates at the specific temperatures were calculated. This is the first systematic study where the self-dissociation of an oligomeric chaperonin as well as its activation parameters are reported.
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Asano, T., and Le Noble, W. J. (1978). Chem. Rev. 78: 407–489.
Balny, C., Masson, P., and Heremans, K. (2002). Biochim. Biophys. Acta. 1595: 3–10.
Balny, C., Masson, P., and Heremans, K. (Eds) (2002). Special Issue: Frontiers in High Pressure Biochemistry and Biophysics, Biophys. Biochim. Acta 1595: Issue 1–2.
Bevington, P. R., and Robinson, D. K. (1992). Data Reduction and Error Analysis for the Physical Sciences, Second Edition, McGraw-Hill, Inc., New York, Ch. 3, pp. 38–52.
Blandamer, M. J., Davis, M. I., Douheret, G., and Reis, J. C. R. (2001). Chem. Soc. Rev. 30: 8–15.
Boisvert, D. C., Wang, J., Otwinowski, Z., Horwich, A. L., and Sigler, P. B. (1996). Nat. Struct. Biol. 3: 170–177.
Bonafe, C. F., Vital, C. M., Telles, R. C., Goncalves, M. C., Matsuura, M. S., Pessine, F. B., Freitas, D. R., and Vega, J. (1998). Biochemistry 37: 11097–11105.
Braig, K., Adams, P. D., and Brunger, A. T. (1995). Nat. Struct. Biol. 2: 1083–1094.
Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D. C., Joachimiak, A., Horwich, A. L., and Sigler, P. B. (1994). Nature 371: 578–586.
Buchner, J., Schmidt, M., Fuchs, M., Jaenicke, R., Rudolph, R., Schmid, F. X., and Kiefhaber, T. (1991). Biochemistry 30: 1586–1591.
Chatellier, J., Hill, F., Foster, N. W., Goloubinoff, P., and Fersht, A. R. (2000). J. Mol. Biol. 304: 897–910.
Cheng, M. Y., Hartl, F. U., Martin, J., Pollock, R. A., Kalousek, F., Neupert, W., Hallberg, E. M., Hallberg, R. L., and Horwick, A. L. (1989). Nature 337: 620–625.
Cioni, P., and Strambini, G. B. (1996). J. Mol. Biol. 263: 789–799.
Clark, A. C., Hugo, E., and Frieden, C. (1996). Biochemistry 35: 5893–5901.
Clark, A. C., Karon, B. S., and Frieden, C. (1999). Protein Sci. 8: 2166–2176.
Drljaca, A., Hubbard, C. D., van Eldik, R., Asano, T., Basilevsky, M. V., and Le Noble, W. J. (1998). Chem. Rev. 98: 2167–2289.
Fayet, O., Ziegelhoffer, T., and Georgopoulos, C. (1989). J. Bacteriol. 171: 1379–1385.
Galan, A., Sot, B., Llorca, O., Carrascosa, J. L., Valpuesta, J. M., and Muga, A. (2001). J. Biol. Chem. 276: 957–964.
Goloubinoff, P., Christeller, J. T., Gatenby, A. A., and Lorimer, G. H. (1989). Nature 342: 884–889.
Gorovits, B. M., and Horowitz, P. M. (1995). J. Biol. Chem. 270: 28551–28556.
Gorovits, B. M., and Horowitz, P. M. (1998). Biochemistry 37: 6132–6135.
Gorovits, B., Raman, C. S., and Horowitz, P. M. (1995). J. Biol. Chem. 270: 2061–2066.
Grallert, H., and Buchner, J. (2001). J. Struct. Biol. 135: 95–103.
Gross, M., and Jaenicke, R. (1994). Eur. J. Biochem. 221: 617–630.
Hayer-Hartl, M. K., Weber, F., and Hartl, F. U. (1996). EMBO J. 15: 6111–6121.
Heremans, K. (1982). Annu. Rev. Biophys. Bioeng. 11: 1–21.
Holzapfel, W. B., and Isaacs, N. (1997). High-Pressure Techniques in Chemistry and Physics. Oxford University Press, New York.
Holzinger, J., Heumann, H., Manakova, E., Rossle, M., Vanatalu, K., Wiedenmann, A., and May, R. P. (2000). Physica B 276–278: 528–529.
Horwich, A. L., Burston, S. G., Rye, H. S., Weissman, J. S., and Fenton, W. A. (1998). Methods Enzymol. 290: 141–146.
Horwich, A. L., Low, K. B., Fenton, W. A., Hirshfield, I. N., and Furtak, K. (1993). Cell 74: 909–917.
Hynes, J. T. (1985). Annu. Rev. Phys. Chem. 36: 573–597.
Jacob, M., and Schmid, F. X. (1999). Biochemistry 38: 13773–13779.
Jannasch, H. W., Marquis, R. E., and Zimmerman, A. M. (eds.) (1987). Current Perspectives in High Pressure Biology, Academic Press, Orlando, FL.
Johnson, F. H., and Eyring, H. (1970). In A. M. Zimmerman (ed.), High Pressure Effects on Cellular Processes, Academic Press, New York, Ch. 1, pp. 1–44.
Kelm, H., and Palmer, D. (1978). In H. Kelm (ed.), High Pressure Chemistry, NATO Adv. Study Inst. Ser., Ser C, Reidel, Dordrecht, pp. 281–309.
Kitahara, R., and Akasaka, K. (2003). Proc. Natl. Acad. Sci. U. S. A. 100: 3167–3172.
Kitahara, R., Kato, M., and Taniguchi, Y. (2003). Protein Sci. 12: 207–217.
Kramers, H. A. (1940). Physica B 7: 284–304.
Laminet, A. A., Ziegelhoffer, T., Georgopoulos, C., and Pluckthun, A. (1990). EMBO J. 9: 2315–2319.
Lassalle, M. W., Yamada, H., and Akasaka, K. (2000). J. Mol. Biol. 298: 293–302.
Lorimer, G. (1997). Nature 388: 720–723.
Markley, J. L., Northrop, D. B., and Royer, C. (1996). High-Pressure Effects in Molecular Biophysics and Enzymology, Oxford University Press, New York.
Martin, J., Langer, T., Boteva, R., Schramel, A., Horwich, A. L., and Hartl, F. U. (1991). Nature 352: 36–42.
Morild, E. (1981). In C. B. Anfinson, Edsall, J. T., and Richards, F. M. (eds.), Advances in Protein Chemistry, Academic Press, New York, Vol. 34, pp. 93–166.
Mozhaev, V. V., Heremans, K., Frank, J., Masson, P., and Balny, C. (1996). Proteins 24: 81–91.
Neuman, R. C. Jr., Kauzman, W., and Zipp, A. (1973). J. Phys. Chem. 77: 2687–2691.
Paladini, A. A., Jr., and Weber, G. (1981). Biochemistry 20: 2587–2593.
Panda, M., and Horowitz, P. M. (2002). Biochemistry 41: 1869–1876.
Panda, M., Ybarra, J., and Horowitz, P. M. (2001). J. Biol. Chem. 276: 6253–6259.
Panda, M., Ybarra, J., and Horowitz, P. M. (2002). Biochemistry 41: 12843–12849.
Prehoda, K. E., Mooberry, E. S., and Markley, J. L. (1998). Biochemistry 37: 5785–5790.
Rietveld, A. W., and Ferreira, S. T. (1996). Biochemistry 35: 7743–7751.
Royer, C. A. (2002). Biochim. Biophys. Acta 1595: 201–209.
Rye, H. S., Burston, S. G., Fenton, W. A., Beechem, J. M., Xu, Z., Sigler, P. B., and Horwich, A. L. (1997). Nature 388: 792–798.
Rye, H. S., Roseman, A. M., Chen, S., Furtak, K., Fenton, W. A., Saibil, H. R., and Horwich, A. L. (1999). Cell 97: 325–338.
Saibil, H. R., Horwich, A. L., and Fenton, W. A. (2002). In Horwich, A. (ed.), Advances in Protein Chemistry, Academic Press, New York, 59, pp. 45–72.
Sandstrom, J. (1982). Dynamic NMR Spectroscopy, Academic Press, New York. Ch. 7, pp 108–123.
Seemann, H., Winter, R., and Royer, C. A. (2001). J. Mol. Biol. 307: 1091–1102.
Sherman, W. F., and Stadtmuller, A. A. (1987). Experimental Techniques in High-Pressure Research, Wiley, Chichester.
Silva, J. L., Foguel, D., and Royer, C. A. (2001). Trends Biochem. Sci. 26: 612–618.
Silva, J. L., and Weber, G. (1993). Annu. Rev. Phys. Chem. 44: 89–113.
St. John, R. J., Carpenter, J. F., and Randolph, T. W. (1999). Proc. Natl. Acad. Sci. U. S. A. 96: 13029–13033.
Tauc, P., Mateo, C. R., and Brochon, J. C. (2002). Biochim. Biophys. Acta 1595: 103–115.
Taulier, N., and Chalikian, T. V. (2002). Biochim. Biophys. Acta 1595: 48–70.
Thirumalai, D., and Lorimer, G. H. (2001). Annu. Rev. Biophys. Biomol. Struct. 30: 245–269.
Torrent, J., Alvarez-Martinez, M. T., Heitz, F., Liautard, J. P., Balny, C., and Lange, R. (2003). Biochemistry 42: 1318–1325.
Trovaslet, M., Dallet-Choisy, S., Meersman, F., Heremans, K., Balny, C., and Legoy, M. D. (2003). Eur. J. Biochem 270: 119–128.
van Eldik, R. (1986). Inorganic High Pressure Chemistry: Kinetics and Mechanisms, Elsevier, Amsterdam.
van Eldik, R., Asano, T., and Le Noble, W. J. (1989). Chem. Rev. 89: 549–688.
van Eldik, R., and Jonas, J. (eds.) (1987). High-Pressure Chemistry and Biochemistry, Reidel, Dordrecht, The Netherlands.
Viitanen, P. V., Lubben, T. H., Reed, J., Goloubinoff, P., O'Keefe, D. P., and Lorimer, G. H. (1990). Biochemistry 29: 5665–5671.
Wang, J., and Boisvert, D. C. (2003). J. Mol. Biol. 327: 843–855.
Webb, J. N., Webb, S. D., Cleland, J. L., Carpenter, J. F., and Randolph, T. W. (2001). Proc. Natl. Acad. Sci. U. S. A. 98: 7259–7264.
Weber, G. (1992). Protein Interactions, Chapman and Hall Inc., New York.
Weber, G. (1993). J. Phy. Chem. 97: 7108–7115.
Weissman, J. S., Hohl, C. M., Kovalenko, O., Kashi, Y., Chen, S., Braig, K., Saibil, H. R., Fenton, W. A., and Horwich, A. L. (1995). Cell 83: 577–587.
Weissman, J. S., Rye, H. S., Fenton, W. A., Beechem, J. M., and Horwich, A. L. (1996). Cell 84: 481–490.
White, Z. W., Fisher, K. E., and Eisenstein, E. (1995). J. Biol. Chem. 270: 20404–20409.
Winter, R., and Jonas, J. (eds.) (1993). High Pressure Chemistry, Biochemistry and Materials Science. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Xu, Z., Horwich, A. L., and Sigler, P. B. (1997). Nature 388: 741–750.
Xu, Z., and Sigler, P. B. (1998). J. Struct. Biol. 124: 129–141.
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Panda, M., Horowitz, P.M. Activation Parameters for the Spontaneous and Pressure-Induced Phases of the Dissociation of Single-Ring GroEL (SR1) Chaperonin. J Protein Chem 23, 85–94 (2004). https://doi.org/10.1023/B:JOPC.0000016262.27420.3a
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DOI: https://doi.org/10.1023/B:JOPC.0000016262.27420.3a