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An obligatory intermediate in the folding pathway of cytochrome c552 from Hydrogenobacter thermophilus.

Travaglini-Allocatelli C, Gianni S, Dubey VK, Borgia A, Di Matteo A, Bonivento D, CutruzzolĂ  F, Bren KL, Brunori M
J Biol Chem 280 25729-34 (2005)
Cited: 40 times
EuropePMC logo PMID: 15883159

Abstract

The folding mechanism of many proteins involves the population of partially organized structures en route to the native state. Identification and characterization of these intermediates is particularly difficult, as they are often only transiently populated and may play different mechanistic roles, being either on-pathway productive species or off-pathway kinetic traps. Following different spectroscopic probes, and employing state-of-the-art kinetic analysis, we present evidence that the folding mechanism of the thermostable cytochrome c552 from Hydrogenobacter thermophilus does involve the presence of an elusive, yet compact, on-pathway intermediate. Characterization of the folding mechanism of this cytochrome c is particularly interesting for the purpose of comparative folding studies, because H. thermophilus cytochrome c552 shares high sequence identity and structural homology with its homologue from the mesophilic bacterium Pseudomonas aeruginosa cytochrome c551, which refolds through a broad energy barrier without the accumulation of intermediates. Analysis of the folding kinetics and correlation with the three-dimensional structure add new evidence for the validity of a consensus folding mechanism in the cytochrome c family.

Reviews - 1ynr mentioned but not cited (3)

  1. The chemistry and biochemistry of heme c: functional bases for covalent attachment. Bowman SE, Bren KL. Nat Prod Rep 25 1118-1130 (2008)
  2. Review: studies of ferric heme proteins with highly anisotropic/highly axial low spin (S = 1/2) electron paramagnetic resonance signals with bis-histidine and histidine-methionine axial iron coordination. Zoppellaro G, Bren KL, Ensign AA, Harbitz E, Kaur R, Hersleth HP, Ryde U, Hederstedt L, Andersson KK. Biopolymers 91 1064-1082 (2009)
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Articles - 1ynr mentioned but not cited (13)

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  3. Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth. Beckwith CR, Edwards MJ, Lawes M, Shi L, Butt JN, Richardson DJ, Clarke TA. Front Microbiol 6 332 (2015)
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  6. Temperature dependent equilibrium native to unfolded protein dynamics and properties observed with IR absorption and 2D IR vibrational echo experiments. Chung JK, Thielges MC, Bowman SE, Bren KL, Fayer MD. J Am Chem Soc 133 6681-6691 (2011)
  7. The influence of heme ruffling on spin densities in ferricytochromes c probed by heme core 13C NMR. Kleingardner JG, Bowman SE, Bren KL. Inorg Chem 52 12933-12946 (2013)
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Reviews citing this publication (3)

  1. Identification and characterization of protein folding intermediates. Gianni S, Ivarsson Y, Jemth P, Brunori M, Travaglini-Allocatelli C. Biophys Chem 128 105-113 (2007)
  2. What lessons can be learned from studying the folding of homologous proteins? Nickson AA, Clarke J. Methods 52 38-50 (2010)
  3. Early events, kinetic intermediates and the mechanism of protein folding in cytochrome C. Goldbeck RA, Chen E, Kliger DS. Int J Mol Sci 10 1476-1499 (2009)

Articles citing this publication (21)

  1. A PDZ domain recapitulates a unifying mechanism for protein folding. Gianni S, Geierhaas CD, Calosci N, Jemth P, Vuister GW, Travaglini-Allocatelli C, Vendruscolo M, Brunori M. Proc Natl Acad Sci U S A 104 128-133 (2007)
  2. The denatured state dictates the topology of two proteins with almost identical sequence but different native structure and function. Morrone A, McCully ME, Bryan PN, Brunori M, Daggett V, Gianni S, Travaglini-Allocatelli C. J Biol Chem 286 3863-3872 (2011)
  3. Variation and analysis of second-sphere interactions and axial histidinate character in c-type cytochromes. Bowman SE, Bren KL. Inorg Chem 49 7890-7897 (2010)
  4. 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)
  5. Domain-swapped dimer of Pseudomonas aeruginosa cytochrome c551: structural insights into domain swapping of cytochrome c family proteins. Nagao S, Ueda M, Osuka H, Komori H, Kamikubo H, Kataoka M, Higuchi Y, Hirota S. PLoS One 10 e0123653 (2015)
  6. Change in structure and ligand binding properties of hyperstable cytochrome c555 from Aquifex aeolicus by domain swapping. Yamanaka M, Nagao S, Komori H, Higuchi Y, Hirota S. Protein Sci 24 366-375 (2015)
  7. Identification and Structural Characterization of an Intermediate in the Folding of the Measles Virus X Domain. Bonetti D, Camilloni C, Visconti L, Longhi S, Brunori M, Vendruscolo M, Gianni S. J Biol Chem 291 10886-10892 (2016)
  8. Insight into the Folding and Dimerization Mechanisms of the N-Terminal Domain from Human TDP-43. Vivoli-Vega M, Guri P, Chiti F, Bemporad F. Int J Mol Sci 21 E6259 (2020)
  9. Influence of heme c attachment on heme conformation and potential. Kleingardner JG, Levin BD, Zoppellaro G, Andersson KK, Elliott SJ, Bren KL. J Biol Inorg Chem 23 1073-1083 (2018)
  10. Electron transfer from cytochrome c to cupredoxins. Takayama SJ, Irie K, Tai H, Kawahara T, Hirota S, Takabe T, Alcaraz LA, Donaire A, Yamamoto Y. J Biol Inorg Chem 14 821-828 (2009)
  11. Oligomerization enhancement and two domain swapping mode detection for thermostable cytochrome c552 via the elongation of the major hinge loop. Ren C, Nagao S, Yamanaka M, Komori H, Shomura Y, Higuchi Y, Hirota S. Mol Biosyst 11 3218-3221 (2015)
  12. Molecular dynamics simulations of Hydrogenobacter thermophilus cytochrome c552: comparisons of the wild-type protein, a b-type variant, and the apo state. Smith LJ, Davies RJ, van Gunsteren WF. Proteins 65 702-711 (2006)
  13. Plasticity of the protein folding landscape: switching between on- and off-pathway intermediates. Gianni S, Brunori M, Travaglini-Allocatelli C. Arch Biochem Biophys 466 172-176 (2007)
  14. Rational Design of Domain-Swapping-Based c-Type Cytochrome Heterodimers by Using Chimeric Proteins. Zhang M, Nakanishi T, Yamanaka M, Nagao S, Yanagisawa S, Shomura Y, Shibata N, Ogura T, Higuchi Y, Hirota S. Chembiochem 18 1712-1715 (2017)
  15. A new cytoplasmic monoheme cytochrome c from Acidithiobacillus ferrooxidans involved in sulfur oxidation. Liu Y, Guo S, Yu R, Zou K, Qiu G. Curr Microbiol 68 285-292 (2014)
  16. Biophysical characterization and folding studies of plant protease, wrightin: identification of folding intermediate under different conditions. Tomar R, Dubey VK, Jagannadham MV. Protein J 28 213-223 (2009)
  17. Cloning, expression and purification of cytochrome c(6) from the brown alga Hizikia fusiformis and complete X-ray diffraction analysis of the structure. Akazaki H, Kawai F, Chida H, Matsumoto Y, Hirayama M, Hoshikawa K, Unzai S, Hakamata W, Nishio T, Park SY, Oku T. Acta Crystallogr Sect F Struct Biol Cryst Commun 64 674-680 (2008)
  18. Stability enhancement of cytochrome c through heme deprotonation and mutations. Sonoyama T, Hasegawa J, Uchiyama S, Nakamura S, Kobayashi Y, Sambongi Y. Biophys Chem 139 37-41 (2009)
  19. Unveiling the folding mechanism of the Bromodomains. Petrosino M, Bonetti D, Pasquo A, Lori L, Chiaraluce R, Consalvi V, Travaglini-Allocatelli C. Biochem Biophys Rep 11 99-104 (2017)
  20. Characterization of N-terminal amino group-heme ligation emerging upon guanidine hydrochloric acid induced unfolding of Hydrogenobacter thermophilus ferricytochrome c552. Tai H, Kawano S, Yamamoto Y. J Biol Inorg Chem 13 25-34 (2008)
  21. 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)


Related citations provided by authors (1)

  1. Solution structure of thermostable cytochrome c-552 from Hydrogenobacter thermophilus determined by 1H-NMR spectroscopy.. Hasegawa J, Yoshida T, Yamazaki T, Sambongi Y, Yu Y, Igarashi Y, Kodama T, Yamazaki K, Kyogoku Y, Kobayashi Y Biochemistry 37 9641-9 (1998)

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