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Replacement of Lysine 45 by Uncharged Residues Modulates the Redox-Bohr Effect in Tetraheme Cytochrome c3 of Desulfovibrio vulgaris (Hildenborough)

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Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Apt. 127, 2780 Oeiras, Portugal, Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia 30602, and Department of Biochemistry, Wageningen Agricultural University, Dreijenlaan 3, 6703 HA Wageningen, The Netherlands
Cite this: Biochemistry 1998, 37, 35, 12160–12165
Publication Date (Web):August 5, 1998
https://doi.org/10.1021/bi981001v
Copyright © 1998 American Chemical Society
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Abstract

The structural basis for the pH dependence of the redox potential in the tetrahemic Desulfovibriovulgaris (Hildenborough) cytochrome c3 was investigated by site-directed mutagenesis of charged residues in the vicinity of heme I. Mutation of lysine 45, located in the neighborhood of the propionates of heme I, by uncharged residues, namely threonine, glutamine and leucine, was performed. The replacement of a conserved charged residue, aspartate 7, present in the N-terminal region and near heme I was also attempted. The analysis of the redox interactions as well as the redox-Bohr behavior of the mutated cytochromes c3 allowed the conclusion that residue 45 has a functional role in the control of the pKa of the propionate groups of heme I and confirms the involvement of this residue in the redox-Bohr effect.

 This work was supported by EU Grants FMRX-CT-98-0218, PRAXIS PCNA BIO/74/96 (AVX), and JCNIT BIA-2164/95 (L.M.S.).

 Universidade Nova de Lisboa.

§

 University of Georgia.

 Wageningen Agricultural University.

*

 To whom correspondence should be addressed. Phone: 351-1-4428616. Fax: 351-1-4428766. E-mail: [email protected]

Cited By


This article is cited by 15 publications.

  1. Joana M. Dantas, Luísa M. Campelo, Norma E. C. Duke, Carlos A. Salgueiro, P. Raj Pokkuluri. The structure of PccH from Geobacter sulfurreducens  - a novel low reduction potential monoheme cytochrome essential for accepting electrons from an electrode. The FEBS Journal 2015, 282 (11) , 2215-2231. https://doi.org/10.1111/febs.13269
  2. Cláudio M. Soares, António M. Baptista. Simulation of multihaem cytochromes. FEBS Letters 2012, 586 (5) , 510-518. https://doi.org/10.1016/j.febslet.2011.10.019
  3. Ricardo O. Louro. Proton thrusters: overview of the structural and functional features of soluble tetrahaem cytochromes c 3. JBIC Journal of Biological Inorganic Chemistry 2006, 12 (1) , 1-10. https://doi.org/10.1007/s00775-006-0165-y
  4. Ana C. Messias, António P. Aguiar, Lorraine Brennan, Carlos A. Salgueiro, Lígia M. Saraiva, António V. Xavier, David L. Turner. Solution structures of tetrahaem ferricytochrome c3 from Desulfovibrio vulgaris (Hildenborough) and its K45Q mutant: The molecular basis of cooperativity. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2006, 1757 (2) , 143-153. https://doi.org/10.1016/j.bbabio.2006.01.007
  5. Naoki Yahata, Kiyoshi Ozawa, Yusuke Tomimoto, Kumiko Morita, Hirofumi Komori, Hideaki Ogata, Yoshiki Higuchi, Hideo Akutsu. Roles of charged residues in pH-dependent redox properties of cytochrome c3 from Desulfovibrio vulgaris Miyazaki F. BIOPHYSICS 2006, 2 , 45-56. https://doi.org/10.2142/biophysics.2.45
  6. Ilídio J. Correia, Catarina M. Paquete, Ana Coelho, Claudia C. Almeida, Teresa Catarino, Ricardo O. Louro, Carlos Frazão, Lígia M. Saraiva, Maria Arménia Carrondo, David L. Turner, António V. Xavier. Proton-assisted Two-electron Transfer in Natural Variants of Tetraheme Cytochromes from Desulfomicrobium Sp.. Journal of Biological Chemistry 2004, 279 (50) , 52227-52237. https://doi.org/10.1074/jbc.M408763200
  7. Vitor H. Teixeira, António M. Baptista, Cláudio M. Soares. Modeling Electron Transfer Thermodynamics in Protein Complexes: Interaction between Two Cytochromes c3. Biophysical Journal 2004, 86 (5) , 2773-2785. https://doi.org/10.1016/S0006-3495(04)74331-3
  8. Isabel Bento, Pedro M. Matias, António M. Baptista, Patricia N. da Costa, Walter M.A.M. van Dongen, Lígia M. Saraiva, Thomas R. Schneider, Cláudio M. Soares, Maria A. Carrondo. Molecular basis for redox-Bohr and cooperative effects in cytochrome c3 from Desulfovibrio desulfuricans ATCC 27774: Crystallographic and modeling studies of oxidized and reduced high-resolution structures at pH 7.6. Proteins: Structure, Function, and Bioinformatics 2004, 54 (1) , 135-152. https://doi.org/10.1002/prot.10431
  9. K.R. Rodgers, G.S. Lukat-Rodgers. Electron Transfer: Cytochromes. 2003,,, 17-60. https://doi.org/10.1016/B0-08-043748-6/08205-0
  10. Oliver Einsle, Stefanie Foerster, Karlheinz Mann, Günter Fritz, Albrecht Messerschmidt, Peter M. H. Kroneck. Spectroscopic investigation and determination of reactivity and structure of the tetraheme cytochrome c 3 from Desulfovibrio desulfuricans Essex 6. European Journal of Biochemistry 2001, 268 (10) , 3028-3035. https://doi.org/10.1046/j.1432-1327.2001.02195.x
  11. P da Costa. Cloning, sequencing and expression of the tetraheme cytochrome c3 from Desulfovibrio gigas. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 2000, 1492 (1) , 271-275. https://doi.org/10.1016/S0167-4781(00)00099-3
  12. Lorraine Brennan, David L. Turner, Ana C. Messias, Miguel L. Teodoro, Jean LeGall, Helena Santos, António V. Xavier. Structural basis for the network of functional cooperativities in cytochrome c3 from Desulfovibrio gigas: solution structures of the oxidised and reduced states. Journal of Molecular Biology 2000, 298 (1) , 61-82. https://doi.org/10.1006/jmbi.2000.3652
  13. Patrı́cia N. da Costa, Cristiano Conte, Lı́gia M. Saraiva. Expression of a Desulfovibrio Tetraheme Cytochrome c in Escherichia coli. Biochemical and Biophysical Research Communications 2000, 268 (3) , 688-691. https://doi.org/10.1006/bbrc.2000.2198
  14. Lı́gia M Saraiva, Patrı́cia N da Costa, Jean LeGall. Sequencing the Gene Encoding Desulfovibrio desulfuricans ATCC 27774 Nine-Heme Cytochrome c. Biochemical and Biophysical Research Communications 1999, 262 (3) , 629-634. https://doi.org/10.1006/bbrc.1999.1238
  15. António M. Baptista, Paulo J. Martel, Cláudio M. Soares. Simulation of Electron-Proton Coupling with a Monte Carlo Method: Application to Cytochrome c3 Using Continuum Electrostatics. Biophysical Journal 1999, 76 (6) , 2978-2998. https://doi.org/10.1016/S0006-3495(99)77452-7

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