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Stability and folding kinetics of structurally characterized cytochrome c-b562.

Faraone-Mennella J, Tezcan FA, Gray HB, Winkler JR
Biochemistry 45 10504-11 (2006)
Cited: 41 times
EuropePMC logo PMID: 16939202

Abstract

The four-helix-bundle protein fold can be constructed from a wide variety of primary amino acid sequences. Proteins with this structure are excellent candidates for investigations of the relationship between folding mechanism and topology. The folding of cytochrome b(562), a four-helix-bundle heme protein, is hampered by heme dissociation. To overcome this complication, we have engineered a variant of cytochrome b(562) (cyt c-b(562)) featuring a c-type linkage between the heme and the polypeptide chain. The replacement of the native cyt b(562) leader sequence in this protein with that of a c-type cytochrome (cyt c(556)) led to high yields of fully matured and correctly folded cyt c-b(562). We have determined the X-ray crystal structure of cyt c-b(562) at 2.25 A and characterized its physical, chemical, and folding properties. These measurements reveal that the c-type linkage does not perturb the protein fold or reduction potential of the heme group. The covalent attachment of the porphyrin to the polypeptide does, however, produce a substantial change in protein stability and folding kinetics.

Articles - 2bc5 mentioned but not cited (13)

  1. Controlled protein dimerization through hybrid coordination motifs. Radford RJ, Nguyen PC, Ditri TB, Figueroa JS, Tezcan FA. Inorg Chem 49 4362-4369 (2010)
  2. Metal-Directed Design of Supramolecular Protein Assemblies. Bailey JB, Subramanian RH, Churchfield LA, Tezcan FA. Methods Enzymol 580 223-250 (2016)
  3. Domain-swapped cytochrome cb562 dimer and its nanocage encapsulating a Zn-SO4 cluster in the internal cavity. Miyamoto T, Kuribayashi M, Nagao S, Shomura Y, Higuchi Y, Hirota S. Chem Sci 6 7336-7342 (2015)
  4. Prospects for de novo phasing with de novo protein models. Das R, Baker D. Acta Crystallogr D Biol Crystallogr 65 169-175 (2009)
  5. Folding energy landscape of cytochrome cb562. Kimura T, Lee JC, Gray HB, Winkler JR. Proc Natl Acad Sci U S A 106 7834-7839 (2009)
  6. Determining the Structural and Energetic Basis of Allostery in a De Novo Designed Metalloprotein Assembly. Churchfield LA, Alberstein RG, Williamson LM, Tezcan FA. J Am Chem Soc 140 10043-10053 (2018)
  7. Multiple Roles of Black Raspberry Anthocyanins Protecting against Alcoholic Liver Disease. Xiao T, Luo Z, Guo Z, Wang X, Ding M, Wang W, Shen X, Zhao Y. Molecules 26 2313 (2021)
  8. Cytochrome unfolding pathways from computational analysis of crystal structures. Kozak JJ, Gray HB, Garza-López RA. J Inorg Biochem 155 44-55 (2016)
  9. Overcoming universal restrictions on metal selectivity by protein design. Choi TS, Tezcan FA. Nature 603 522-527 (2022)
  10. Funneled angle landscapes for helical proteins. Kozak JJ, Gray HB, Garza-López RA. J Inorg Biochem 208 111091 (2020)
  11. Intrachain contact dynamics in unfolded cytochrome cb562. Bouley Ford ND, Shin DW, Gray HB, Winkler JR. J Phys Chem B 117 13206-13211 (2013)
  12. Computationally Guided Redesign of a Heme-free Cytochrome with Native-like Structure and Stability. Hoffnagle AM, Eng VH, Markel U, Tezcan FA. Biochemistry 61 2063-2072 (2022)
  13. Unfolding cytochromes c-b562 and Rd apo b562. Kozak JJ, Gray HB, Garza-López RA. J Inorg Biochem 211 111209 (2020)


Reviews citing this publication (2)

  1. Metal-directed protein self-assembly. Salgado EN, Radford RJ, Tezcan FA. Acc Chem Res 43 661-672 (2010)
  2. Hemoprotein-based supramolecular assembling systems. Oohora K, Hayashi T. Curr Opin Chem Biol 19 154-161 (2014)

Articles citing this publication (26)

  1. A designed supramolecular protein assembly with in vivo enzymatic activity. Song WJ, Tezcan FA. Science 346 1525-1528 (2014)
  2. Metal templated design of protein interfaces. Salgado EN, Ambroggio XI, Brodin JD, Lewis RA, Kuhlman B, Tezcan FA. Proc Natl Acad Sci U S A 107 1827-1832 (2010)
  3. Development of a heme protein structure-electrochemical function database. Reedy CJ, Elvekrog MM, Gibney BR. Nucleic Acids Res 36 D307-13 (2008)
  4. Controlling protein-protein interactions through metal coordination: assembly of a 16-helix bundle protein. Salgado EN, Faraone-Mennella J, Tezcan FA. J Am Chem Soc 129 13374-13375 (2007)
  5. Exceptionally stable, redox-active supramolecular protein assemblies with emergent properties. Brodin JD, Carr JR, Sontz PA, Tezcan FA. Proc Natl Acad Sci U S A 111 2897-2902 (2014)
  6. Metal-mediated self-assembly of protein superstructures: influence of secondary interactions on protein oligomerization and aggregation. Salgado EN, Lewis RA, Faraone-Mennella J, Tezcan FA. J Am Chem Soc 130 6082-6084 (2008)
  7. Constructing a man-made c-type cytochrome maquette in vivo: electron transfer, oxygen transport and conversion to a photoactive light harvesting maquette. Anderson JLR, Armstrong CT, Kodali G, Lichtenstein BR, Watkins DW, Mancini JA, Boyle AL, Farid TA, Crump MP, Moser CC, Dutton PL. Chem Sci 5 507-514 (2014)
  8. Constructing protein polyhedra via orthogonal chemical interactions. Golub E, Subramanian RH, Esselborn J, Alberstein RG, Bailey JB, Chiong JA, Yan X, Booth T, Baker TS, Tezcan FA. Nature 578 172-176 (2020)
  9. In vitro and cellular self-assembly of a Zn-binding protein cryptand via templated disulfide bonds. Medina-Morales A, Perez A, Brodin JD, Tezcan FA. J Am Chem Soc 135 12013-12022 (2013)
  10. Resonant inelastic X-ray scattering on ferrous and ferric bis-imidazole porphyrin and cytochrome c: nature and role of the axial methionine-Fe bond. Kroll T, Hadt RG, Wilson SA, Lundberg M, Yan JJ, Weng TC, Sokaras D, Alonso-Mori R, Casa D, Upton MH, Hedman B, Hodgson KO, Solomon EI. J Am Chem Soc 136 18087-18099 (2014)
  11. Structural characterization of a microperoxidase inside a metal-directed protein cage. Ni TW, Tezcan FA. Angew Chem Int Ed Engl 49 7014-7018 (2010)
  12. An efficient, step-economical strategy for the design of functional metalloproteins. Rittle J, Field MJ, Green MT, Tezcan FA. Nat Chem 11 434-441 (2019)
  13. Site-specific collapse dynamics guide the formation of the cytochrome c' four-helix bundle. Kimura T, Lee JC, Gray HB, Winkler JR. Proc Natl Acad Sci U S A 104 117-122 (2007)
  14. Control of DegP-dependent degradation of c-type cytochromes by heme and the cytochrome c maturation system in Escherichia coli. Gao T, O'Brian MR. J Bacteriol 189 6253-6259 (2007)
  15. Snapshots of a protein folding intermediate. Yamada S, Bouley Ford ND, Keller GE, Ford WC, Gray HB, Winkler JR. Proc Natl Acad Sci U S A 110 1606-1610 (2013)
  16. Geometric constraints for porphyrin binding in helical protein binding sites. Negron C, Fufezan C, Koder RL. Proteins 74 400-416 (2009)
  17. Metal-Templated Design of Chemically Switchable Protein Assemblies with High-Affinity Coordination Sites. Kakkis A, Gagnon D, Esselborn J, Britt RD, Tezcan FA. Angew Chem Int Ed Engl 59 21940-21944 (2020)
  18. Modular and versatile hybrid coordination motifs on alpha-helical protein surfaces. Radford RJ, Nguyen PC, Tezcan FA. Inorg Chem 49 7106-7115 (2010)
  19. Stereochemistry of residues in turning regions of helical proteins. Kozak JJ, Gray HB. J Biol Inorg Chem 24 879-888 (2019)
  20. Structural and functional insights into thermally stable cytochrome c' from a thermophile. Fujii S, Oki H, Kawahara K, Yamane D, Yamanaka M, Maruno T, Kobayashi Y, Masanari M, Wakai S, Nishihara H, Ohkubo T, Sambongi Y. Protein Sci 26 737-748 (2017)
  21. Formation and carbon monoxide-dependent dissociation of Allochromatium vinosum cytochrome c' oligomers using domain-swapped dimers. Yamanaka M, Hoshizumi M, Nagao S, Nakayama R, Shibata N, Higuchi Y, Hirota S. Protein Sci 26 464-474 (2017)
  22. Molecular modeling of cytochrome b₅ with a single cytochrome c-like thioether linkage. Lin YW, Wu YM, Liao LF, Nie CM. J Mol Model 18 1553-1560 (2012)
  23. Metals coordinate protein-protein interactions. Kerman K, Kraatz HB. Angew Chem Int Ed Engl 47 6522-6524 (2008)
  24. Comparison of the backbone dynamics of wild-type Hydrogenobacter thermophilus cytochrome c(552) and its b-type variant. Tozawa K, Ferguson SJ, Redfield C, Smith LJ. J Biomol NMR 62 221-231 (2015)
  25. Design of a Flexible, Zn-Selective Protein Scaffold that Displays Anti-Irving-Williams Behavior. Choi TS, Tezcan FA. J Am Chem Soc 144 18090-18100 (2022)
  26. Design of metal-mediated protein assemblies via hydroxamic acid functionalities. Subramanian RH, Zhu J, Bailey JB, Chiong JA, Li Y, Golub E, Tezcan FA. Nat Protoc 16 3264-3297 (2021)


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