Electrostatic Match-making

Carlos H. Faerman, Daniel R. RipollĪ, Corey L. Strickland and P. Andrew Karplus Biochemistry, Molecular and Cell Biology and ĪCornell Theory Center Cornell University, Ithaca, NY 14853

Two structurally related disulfide metabolites, the well-known glutathione (GSSG) and its analog trypanothione (TS2), which is found in trypanosomatid parasites, have different net charges of -2 (GSSG) and +1 (TS2). Three structurally known enzymes which reduce these substrates, human glutathione reductase (hGR), Escherichia coli glutathione reductase (ecGR) and Crithidia fasciculata trypanothione reductase (cfTR) show differential specificity (kcat/Km) for GSSG versus TS2 of 104:1, 102:1 and 10-8:1, respectively. In the figure, the electrostatic isopotential surfaces in the active sites of these enzymes are color coded according to the value of the potential: dark blue 3< f; light blue 0< f< 3; green -1.5< f< 0; yellow -3

This clearly shows an electrostatic preference of hGR for GSSG over TS2. The electrostatic gradient of hGR (not shown) will attract GSSG toward the active site. It has been shown experimentally that hGR can be engineered into a trypanothione reductase (TR) [1], thus changing the relative selectivity for GSSG over TS2. Panel b) displays the isopotentials for hGR(A34E:R37W), respectively. The change in the isopotential surfaces after the double mutation illustrates the electrostatic complementarity between the mutated enzyme and TS2 and is consistent with the increased selectivity (103) of this mutated enzyme toward TS2. E. Coli GR , on the other hand, shows less selectivity for GSSG over TS2 (2x102). By mutating three residues, A18E:N21W:R22N, E. Coli GR specificity for TS2 was increased [2]. Panels c) and d) display the corresponding isopotentials calculated for E. Coli GR(wild type) and E.Coli (A18E:N21W:R22N). The appearence of additional attractive isopotentials for TS2 is apparent. TR shows an exquisite selectivity for TS2 over GSSG by a factor of 108. A triple mutant of TR, TR(E18A:W21R:A343R) [3], acquired GR activity, changing the relative selectivity for TS2 over GSSG by 107. Panels e) and f) show the corresponding electrostatic potentials for both TR(E18A:W21R:A343R) and TR, respectively.

The above examples illustrate the electrostatic complementarity between GR and GSSG and TR and TSST, their natural substrates. Furthermore, electrostatic isopotentials follow the changes in substrate selectivity upon specific mutations.

References

  • [1] G. B. Henderson, P. Ulrich, A. H. Fairlamb and A. Cerami. J. Chem. Soc. Chem. Commun. 593 (1986).

  • [2] M. Bradley, U. S. BŸcheler and C. T. Walsh. Biochemistry 30, 6124-6127 (1991).

  • [3] G. H. Henderson, N. J. Murgolo, J. Kuriyan, K. Osapay, D. Kominos, A. Berry, N. S. Scrutton, N. W. Hinchliffe, R. N. Perham and A. Cerami. Proc. Natl. Acad. Sci. USA 88, 8769-8773 (1991).

  • [4] F. X. Sullivan, S. B. Sobolov, M. Bradley and C. T. Walsh. Biochemistry 30, 2761-2767 (1991).