Journal of Protein Chemistry

, Volume 20, Issue 3, pp 203–215 | Cite as

A Study of the Influence of the Hydrophobic Core Residues of Yeast Iso-2-cytochrome c on Phosphate Binding: A Probe of the Hydrophobic Core-Surface Charge Interactions

  • Hiroshi Taniuchi
  • Ying Shi
  • Gloria I. San Miguel
  • James A. Ferretti
  • James W. Mack
  • Alice Fisher
  • Mona Shah
  • Alan N. Schechter
  • Joseph Shiloach
Article

Abstract

To gain insight into the role of hydrophobic core-surface charge interactions in stabilizing cytochrome c, we investigated the influence of hydrophobic core residues on phosphate binding by mutating residues in yeast iso-2-cytochrome c to those corresponding to iso-1-cytochrome c in various combinations. Heat transition of ultraviolet CD was followed as a function of pH in the presence and absence of phosphate. Thermodynamic parameters were deduced. It was found that the I20V/V43A/M98L mutation in the hydrophobic core, whose locations are remote from the putative phosphate sites, modulates phosphate interactions. The modulation is pH dependent. The I20V/M98L and V43A mutation effects are nonadditive. The results lead to a model analogous to that of Tsao, Evans, and Wennerstrom, where a domain associated with the ordered hydrophobic core is sensitive to the fields generated by the surface charges. Such an explanation would be in accord with the observed difference in thermal stability between iso-2 and horse cytochromes c.

Modulation of phosphate binding influence of hydrophobic core residues electrostatic core-surface interactions polarizable domain model cytochrome c chimeras 

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REFERENCES

  1. Anderson, T., Thulin, E., and Forsen, S. (1979). Biochemistry 18, 2487–2493.Google Scholar
  2. Banci, L., Bertini, I., Gray, H. B., Luciant, C., Reddig, T., Rosato, A., and Turano P. (1997). Biochemistry 36, 9867–9877.Google Scholar
  3. Becktel, W. J. and Schellman, J. A. (1987). Bioplymers 26, 1859–1877.Google Scholar
  4. Berghuis, A. M. and Brayer, G. D. (1992). J.Mol.Biol. 223, 959–976.Google Scholar
  5. Bernstein, F. C., Koetzle, T. F., Williams, G. T. B., Meyer, E. F., Jr., Brile, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T., and Tasumi, M. (1977). J.Mol.Biol. 112, 535–542.Google Scholar
  6. Brautigan, D. L., Ferguson-Miller, S., and Margoliash, E. (1978). J. Biol.Chem. 253, 130–139.Google Scholar
  7. Bushnell, G. W., Louie, G. V., and Brayer, G. D. (1990). J.Mol.Biol. 24, 585–595.Google Scholar
  8. Chen, B.-L. and Shellman, A. (1989). Biochemistry 28, 685–691.Google Scholar
  9. Chen, J., Lu, Z., Sakon, J., and Stites, W. E. (2000). J.Mol.Biol. 303, 125–130.Google Scholar
  10. Chun, P. W. (1996). J.Phys.Chem. 100, 7283–7292.Google Scholar
  11. Cohen, D. S. and Pielak, G. J. (1994). Protein Sci. 3, 1253–1260.Google Scholar
  12. Cox, J. D., Hunt, J. A., Compher, K. M., Fierke, C. A., and Christianson, D. W. (2000). Biochemistry 39, 13687–13694.Google Scholar
  13. Das, G., Sherman, F., Brayer, G. D., and McLendon, G. (1980). Proc. Natl.Acad.Sci.USA 77, 541–545.Google Scholar
  14. Dill, K. A., and Stigter, D. (1995). Adv.Protein Chem. 46, 59–104.Google Scholar
  15. Elwell, M. L. and Schellman, J. A. (1977). Biochim.Biophys.Acta 494, 367–383.Google Scholar
  16. Eriksson, A. E., Baase, W. A., Zhang, X.-J., Heinz, D. W., Blaber, M., Baldwin, E. P., and Matthews, B. W. (1992). Science 255, 178–183.Google Scholar
  17. Fauchere, J.-L. and Pliska, V. (1983). Eur.J.Med.Chem. 18, 369–375.Google Scholar
  18. Faye, G., Leung, D. W., Tatchell, K., Hull, B. D., and Smith, M. (1981). Proc.Natl.Acad.Sci.USA 78, 2258–2262.Google Scholar
  19. Fersht, A. R., Matouschek, A., and Serrano, L. (1992). J.Mol.Biol. 224, 771–782.Google Scholar
  20. Fisher, A. and Taniuchi, H. (1992). Arch.Biochem.Biophys. 296, 1–16.Google Scholar
  21. Fisher, A., Shi, Y., Ritter, A., Ferretti, J. A., Perez-Lamboy, G., Shah, M., Shiloach, J., and Taniuchi, H. (2000). Biochem.Genet. 38, 177–196.Google Scholar
  22. Fleming, P. J. and Richards, F. M. (2000). J.Mol.Biol. 299, 487–498.Google Scholar
  23. Hagihara, Y., Tan, Y., and Goto, Y. (1994). J.Mol.Biol. 237, 336–348.Google Scholar
  24. Hickey, D. R., Berguis, A. M., Lafond, G., Jaeyer, J. A., Cardillo, T. S., McLendon, D., Das, G., Sherman, F., Brayer, G. D., and McLendon, G. (1991). J.Biol.Chem. 266, 11686–11694.Google Scholar
  25. Ikai, A., Fish, W. W., and Tanford, C. (1973). J.Mol.Biol. 73, 165–184.Google Scholar
  26. Jaenicke, R. and Böhm, G. (1998). Curr.Opin.Struct.Biol. 8, 738–748.Google Scholar
  27. Juillerat, M. A. and Taniuch, H. (1982). Proc.Natl.Acad.Sci.USA 79, 1825–1820.Google Scholar
  28. Juillerat, M. A. and Taniuchi, H. (1986). J.Biol.Chem. 261, 2697–2711.Google Scholar
  29. Juillerat, M. A., Parr, G., and Taniuchi, H. (1980). J.Biol.Chem. 255, 845–853.Google Scholar
  30. Kayushin, L. P. and Ajipa, Y. I. (1973). Ann.NY Acad.Sci. 222, 255–265.Google Scholar
  31. Knapp, J. A. and Pace, C. N. (1974). Biochemistry 13, 1284–1294.Google Scholar
  32. Kraulis, P. (1991). J.Appl.Crystallogr. 24, 946–950.Google Scholar
  33. Laemmli, U. K. (1970). Nature 227, 680–685.Google Scholar
  34. Lederer, F., Simmon, A. M., and Verdiere, J. (1972). Biochem.Biophys. Res.Commun. 47, 55–58.Google Scholar
  35. LiCata, V. J. and Ackers, G. K. (1995). Biochemistry 34, 3133–3139.Google Scholar
  36. Liggins, J. R., Sherman, F., Mathew, A. J., and Nall, B. T. (1994). Biochemistry 33, 9209–9219.Google Scholar
  37. Linderstrom-Lang, K. U. and Schellman, J. A. (1959). In The Enzymes (Boyer, P. D., Lardy, H., and Myrback, K., eds.), 2nd ed., Vol. I, Academic Press, San Diego, California, pp. 443–510.Google Scholar
  38. Liu, R., Baase, W. A., and Matthews, B. W. (1999). J.Mol.Biol. 295, 127–145.Google Scholar
  39. Lo, T. P., Guillementte, J. G., Louie, G. V., Smith, M., and Brayer, G. D. (1995a). Biochemistry 34, 163–171.Google Scholar
  40. Lo, T. P., Komar-Panicucci, S., Sherman, F., McLendon, G., and Brayer, G. D. (1995b). Biochemistry 34, 5259–5268.Google Scholar
  41. Louie, G. V. and Brayer, G. D. (1990). J.Mol.Biol. 214, 527–595.Google Scholar
  42. Margalit, R. and Schejter, A. (1973). Eur.J.Biochem. 32, 500–505.Google Scholar
  43. Margoliash, E., Smith, E. L., Kreil, G., and Tuppy, H. (1961). Nature 192, 1121–1127.Google Scholar
  44. Margoliash, E., Barlow, G. H., and Byers, V. (1970). Nature 228, 723–726.Google Scholar
  45. Marmorino, J. L. and Pielak, G. I. (1995). Biochemistry 34, 3140–3143.Google Scholar
  46. McGee, W. A. and Nall, B. T. (1998). Protein Sci. 7, 1071–1082.Google Scholar
  47. McGee, W. A., Rosell, F. I., Liggins, J. R., Rodriguez-Ghidarpour, S., Luo, Y., Chen, J., Brayer, G. D., Mauk, A. G., and Nall, B. T. (1996). Biochemistry 35, 1995–2007.Google Scholar
  48. McLendon, G. and Smith, M. (1978). J.Biol.Chem. 253, 4004–4008.Google Scholar
  49. Montgomery, D. L., Leung, D. W., Smith, M., Shalit, P., Faye, G., and Hull, B. D. (1980). Proc.Natl.Acad.Sci.USA 77, 541–545.Google Scholar
  50. Moore, G. R. and Pettigrew, G. W. (1987). Cytochromes c: Biological Aspects, Springer-Verlag, Berlin.Google Scholar
  51. Moore, G. R. and Pettigrew, G. W. (1990). Cytochromes c: Evolutionary, Structural and Physicochemical Aspects, Springer-Verlag, Berlin.Google Scholar
  52. Murphy, M. E. P., Nall, B. T., and Brayer, G. D. (1992). J.Mol.Biol. 227, 160–176.Google Scholar
  53. Nall, B. T. (1996). In Cytochrome c (Scott, R. A., and Mauk, A. G., eds.),University Science Books, Sausalito, California, pp. 167–200.Google Scholar
  54. Nall, B. T. and Landers, T. A. (1981). Biochemistry 20, 5403–5411.Google Scholar
  55. Narita, K. and Titani, K. (1969). J.Biochem. 65, 259–267.Google Scholar
  56. Osheroff, N., Koppenol, W. H., and Margoliash, E. (1980). J.Biol. Chem. 255, 1689–1697.Google Scholar
  57. Pace, C. N., Shirley, B. A., and Thomson, J. A. (1989). In Protein Structure: A Practical Approach (Creighton, T. E., ed.), IRL Press, Oxford, pp. 311–330.Google Scholar
  58. Parker, D., Davis, A., and Taniuchi, H. (1981). J.Biol.Chem. 256, 4557–4569.Google Scholar
  59. Parr, G. and Taniuchi, H. (1982). J.Biol.Chem. 257, 10103–10111.Google Scholar
  60. Parr, G. and Taniuchi, H. (1983). J.Biol.Chem. 258, 3759–3763.Google Scholar
  61. Parr, G., Hantgan, R., and Taniuchi, H. (1978). J.Biol.Chem. 253, 5381–5388.Google Scholar
  62. Pelletier, H. and Kraut, J. (1992). Science 258, 1748–1755.Google Scholar
  63. Picur, B., Liskowski, M., Taniuchi, H., and Poerio, E. (1994). Arch. Biochem.Biophys. 315, 533–547.Google Scholar
  64. Poerio, E., Parr, G., and Taniuchi, H. (1986). J.Biol.Chem. 261, 10976–10989.Google Scholar
  65. Privalov, P. L. and Khechinashvili, N. N. (1974). J.Mol.Biol. 86, 665–684.Google Scholar
  66. Privalov, P. L. and Makhatadze, G. I. (1990). J.Mol.Biol. 213, 386–391.Google Scholar
  67. Qi, P. X., Beckman, R. A., and Wand, A. L. (1996). Biochemistry 35, 12275–12286.Google Scholar
  68. Schechter, E. and Saludjian, P. (1967). Biopolymer 5, 788–790.Google Scholar
  69. Schellman, J. A. (1975). Biopolymers 14, 999–1018.Google Scholar
  70. Stellwagen, E. and Shulman, R. G. (1973). J.Mol.Biol. 75, 683–695.Google Scholar
  71. Taborsky, G. and McCollum, K. (1979). J.Biol.Chem. 254, 7069–7075.Google Scholar
  72. Takano, T. and Dickerson, R. E. (1981). J.Mol.Biol. 153, 95–115.Google Scholar
  73. Takano, T., Kallai, O. B., Swanson, R., and Dickerson, R. E. (1973). J.Biol.Chem. 248, 5234–5255.Google Scholar
  74. Taniuchi, H. and Fisher, A. (1993). In Peptides: Biology and Chemistry (Du, Y.-C., Tam, J. P., and Zhang, Y.-S., eds.), ESCOM, Leiden, pp. 199–203.Google Scholar
  75. Tsao, Y.-H., Evans, D. F., and Wennerstrom, H. (1993a). Langmuir 9, 779–785.Google Scholar
  76. Tsao, Y.-H., Evans, D. F., and Wennerstrom, H. (1993b). Science 262, 547–550.Google Scholar
  77. Tsong, T. Y. (1976). Biochemistry 15, 5467–5473.Google Scholar
  78. Wada, A. (1976). Adv.Biophys. 9, 1–63.Google Scholar
  79. Warshel, A., Sussman, F., and King, G. (1986). Biochemistry 25, 8368–8372.Google Scholar
  80. Yang, A.-S. and Honig B. (1993). J.Mol.Biol. 231, 459–474.Google Scholar
  81. Yaoi, Y. (1967). J.Biochem. 61, 54–58.Google Scholar
  82. Zuniga, E. H. and Nall, B. T. (1983). Biochemistry 22, 1430–1437.Google Scholar

Copyright information

© Plenum Publishing Corporation 2001

Authors and Affiliations

  • Hiroshi Taniuchi
    • 1
  • Ying Shi
    • 1
  • Gloria I. San Miguel
    • 1
  • James A. Ferretti
    • 2
  • James W. Mack
    • 2
    • 3
  • Alice Fisher
    • 1
  • Mona Shah
    • 1
  • Alan N. Schechter
    • 1
  • Joseph Shiloach
    • 4
  1. 1.Laboratory of Chemical BiologyNational Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of HealthBethesda
  2. 2.Center for Advanced Research of BiotechnologyRockville
  3. 3.Department of BiochemistryHoward University College of MedicineWashington, D.C
  4. 4.Laboratory of Cellular and Development BiologyNational Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of HealthBethesda

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