Role of Aromatic Residues in Stabilization of the [Fe4S4] Cluster in High-potential Iron Proteins (HiPIPs): Physical Characterization and Stability Studies of Tyr-19 Mutants of Chromatium Vinosum HiPIP

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1995 Oct 10

PMID 7568150

Citations 15

Authors

A Agarwal

D Li

J A Cowan

Affiliations

Soon will be listed here.

Abstract

The functional role of residue Tyr-19 of Chromatium vinosum HiPIP has been evaluated by site-directed mutagenesis experiments. The stability of the [Fe4S4] cluster prosthetic center is sensitive to side-chain replacements. Polar residues result in significant instability, while nonpolar residues (especially with aromatic side chains) maintain cluster stability. Two-dimensional NMR data of native and mutant HiPIPs are consistent with a model where Tyr-19 serves to preserve the structural rigidity of the polypeptide backbone, thereby maintaining a hydrophobic barrier for exclusion of water from the cluster cavity. Solvent accessibility results in more facile oxidation of the cluster by atmospheric oxygen, with subsequent rapid hydrolysis of the [Fe4S4]3+ core.

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References

Stoesz J, Redfield A . Cross relaxation and spin diffusion effects on the proton NMR of biopolymers in H2O. Solvent saturation and chemical exchange in superoxide dismutase. FEBS Lett. 1978; 91(2):320-4. DOI: 10.1016/0014-5793(78)81201-0. View

Tedro S, Meyer T, Bartsch R, Kamen M . Primary structures of high potential, four-iron-sulfur ferredoxins from the pruple sulfur photosynthetic bacteria, Thiocapsa roseopersicina and chromatium gracile. J Biol Chem. 1981; 256(2):731-5. View

Kunkel T, Roberts J, Zakour R . Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987; 154:367-82. DOI: 10.1016/0076-6879(87)54085-x. View

Bartsch R . Purification of (4Fe-4S)1--2--ferredoxins (high-potential iron--sulfur proteins) from bacteria. Methods Enzymol. 1978; 53:329-40. DOI: 10.1016/s0076-6879(78)53038-3. View

Bruice T, Maskiewicz R, Job R . The Acid-Base Properties, Hydrolytic Mechanism, and Susceptibility to O(2) Oxidation of Fe(4)S(4)(SR)(4) Clusters. Proc Natl Acad Sci U S A. 1975; 72(1):231-4. PMC: 432277. DOI: 10.1073/pnas.72.1.231. View

Emptage M, Kent T, Kennedy M, BEINERT H, Munck E . Mössbauer and EPR studies of activated aconitase: development of a localized valence state at a subsite of the [4Fe-4S] cluster on binding of citrate. Proc Natl Acad Sci U S A. 1983; 80(15):4674-8. PMC: 384106. DOI: 10.1073/pnas.80.15.4674. View

Langen R, Jensen G, Jacob U, Stephens P, Warshel A . Protein control of iron-sulfur cluster redox potentials. J Biol Chem. 1992; 267(36):25625-7. View

Gaillard J, Albrand J, Moulis J, Wemmer D . Sequence-specific assignments of the 1H nuclear magnetic resonance spectra of reduced high-potential ferredoxin (HiPIP) from Chromatium vinosum. Biochemistry. 1992; 31(24):5632-9. DOI: 10.1021/bi00139a029. View

Jensen G, Warshel A, Stephens P . Calculation of the redox potentials of iron-sulfur proteins: the 2-/3-couple of [Fe4S*4Cys4] clusters in Peptococcus aerogenes ferredoxin, Azotobacter vinelandii ferredoxin I, and Chromatium vinosum high-potential iron protein. Biochemistry. 1994; 33(36):10911-24. DOI: 10.1021/bi00202a010. View

10.

Dutton P . Redox potentiometry: determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems. Methods Enzymol. 1978; 54:411-35. DOI: 10.1016/s0076-6879(78)54026-3. View

11.

Higuchi Y, Yasuoka N, Kakudo M, Katsube Y, Yagi T, Inokuchi H . Single crystals of hydrogenase from Desulfovibrio vulgaris Miyazaki F. J Biol Chem. 1987; 262(6):2823-5. View

12.

SANGER F, Nicklen S, Coulson A . DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977; 74(12):5463-7. PMC: 431765. DOI: 10.1073/pnas.74.12.5463. View

13.

Martin A, Burgess B, Stout C, Cash V, Dean D, Jensen G . Site-directed mutagenesis of Azotobacter vinelandii ferredoxin I: [Fe-S] cluster-driven protein rearrangement. Proc Natl Acad Sci U S A. 1990; 87(2):598-602. PMC: 53312. DOI: 10.1073/pnas.87.2.598. View

14.

Cunningham R, Asahara H, Bank J, Scholes C, Salerno J, Surerus K . Endonuclease III is an iron-sulfur protein. Biochemistry. 1989; 28(10):4450-5. DOI: 10.1021/bi00436a049. View

15.

Rayment I, Wesenberg G, Meyer T, Cusanovich M, Holden H . Three-dimensional structure of the high-potential iron-sulfur protein isolated from the purple phototrophic bacterium Rhodocyclus tenuis determined and refined at 1.5 A resolution. J Mol Biol. 1992; 228(2):672-86. DOI: 10.1016/0022-2836(92)90849-f. View

16.

Carter Jr C, KRAUT J, FREER S, Alden R . Comparison of oxidation-reduction site geometries in oxidized and reduced Chromatium high potential iron protein and oxidized Peptococcus aerogenes ferredoxin. J Biol Chem. 1974; 249(19):6339-46. View

17.

Adman E, Watenpaugh K, Jensen L . NH---S hydrogen bonds in Peptococcus aerogenes ferredoxin, Clostridium pasteurianum rubredoxin, and Chromatium high potential iron protein. Proc Natl Acad Sci U S A. 1975; 72(12):4854-8. PMC: 388830. DOI: 10.1073/pnas.72.12.4854. View

18.

Maskiewicz R, Bruice T . Dependence of the rates of dissolution of the Fe4S4 clusters of Chromatium vinosum high-potential iron protein and ferredoxin on cluster oxidation state. Proc Natl Acad Sci U S A. 1977; 74(12):5231-4. PMC: 431659. DOI: 10.1073/pnas.74.12.5231. View

19.

Job R, Bruice T . Iron-sulfur clusters II: Kinetics of ligand exchange studied on a water-soluble Fe(4)S(4)(SR)(4) cluster. Proc Natl Acad Sci U S A. 1975; 72(7):2478-82. PMC: 432790. DOI: 10.1073/pnas.72.7.2478. View

20.

Peisach J, Mims W, Orme-Johnson W . Linear electric field effect and nuclear modulation studies of ferredoxins and high potential iron-sulfur proteins. J Biol Chem. 1977; 252(16):5643-50. View