Effect of methionine80 heme coordination on domain swapping of cytochrome c

  • Shun Hirota
  • Nobuhiro Yamashiro
  • Zhonghua Wang
  • Satoshi Nagao
Original Paper
First Online:
Received:
Accepted:
Part of the following topical collections:
  1. AsBIC8: 8th Asian Biological Inorganic Chemistry Special Issue

Abstract

Cytochrome c (cyt c) forms oligomers by domain swapping. It exchanges the C-terminal α-helical region between protomers, and the Met80‒heme iron bond is perturbed significantly in domain-swapped oligomers. The peroxidase activity of cyt c increases by Met80 dissociation from the heme iron, which may trigger apoptosis. This study elucidates the effect of the Met80 heme coordination on cyt c domain swapping by obtaining oligomers for both wild-type (WT) and M80A human cyt c by an addition of ethanol to their monomers, followed by lyophilization and dissolution to buffer, and investigating their dimer properties. The absorption and circular dichroism spectra of WT and M80A cyt c exhibited similar changes upon dimerization, indicating that Met80 does not affect the oligomerization process significantly. According to differential scanning calorimetric measurements, Met80 coordination to the heme iron had an effect on the stabilization of the monomer (ΔH = 16 kcal/mol), whereas no large difference was observed between the dimer-to-monomer dissociation temperatures of WT and M80A cyt c (61.0 °C). The activation enthalpy values were similar and relatively large for the dissociation of both WT and M80A cyt c dimers (WT, 120 ± 10 kcal/mol; M80A, 110 ± 10 kcal/mol), indicating that the dimers suffered large structural changes upon dissociation to monomers independent of the Met80 coordination to the heme iron. These results indicate that cyt c domain swapping may occur regardless of the Met80 coordination, whereas the monomer is stabilized by Met80 but the domain-swapped dimer structure and stability are less affected by the Met80 coordination.

Keywords

Cytochrome c Domain swapping Methionine coordination Oligomerization 

Abbreviations

CD

Circular dichroism

Cyt

Cytochrome

DSC

Differential scanning calorimetry

FPLC

Fast protein liquid chromatography

HT

Hydrogenobacter thermophilus

ΔH

Enthalpy change

ΔH‡

Activation enthalpy

PA

Pseudomonas aeruginosa

K

Rate constant

ΔS‡

Activation entropy

SEC

Size exclusion chromatography

Tm

Dissociation temperature

WT

Wild-type

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Notes

Acknowledgements

We thank Mr. Leigh McDowell, Nara Institute of Science and Technology, for his advice on manuscript preparation. This work was partially supported by Grants-in-Aid for Scientific Research from JSPS (Category B, No. JP26288080, S.H.; Challenging Exploratory Research, No. JP15K13744, S.H.; Scientific Research on Innovative Areas, No. JP16H00839, S.H.; Young Scientists B, No. JP16K17935, S.N.), Natural Science Foundation of Sichuan Province of China (No. 11ZB029, Z.W.), Open Project of Chemical Synthesis and Pollution Control Key Laboratory of Sichuan Province (No. CSPC2011-7-2, Z.W.), and Doctoral Fund of China West Normal University (No. 07B011, Z.W.).

Supplementary material

775_2017_1446_MOESM1_ESM.pdf (203 kb)
Supplementary material 1 (PDF 204 kb)

References

  1. 1.
    Spierings D, McStay G, Saleh M, Bender C, Chipuk J, Maurer U, Green DR (2005) Science 310:66–67CrossRefPubMedGoogle Scholar
  2. 2.
    Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cell 91:479–489CrossRefPubMedGoogle Scholar
  3. 3.
    Dickerson RE, Takano T, Eisenberg D, Kallai OB, Samson L, Cooper A, Margoliash E (1971) J Biol Chem 246:1511–1535PubMedGoogle Scholar
  4. 4.
    Bushnell GW, Louie GV, Brayer GD (1990) J Mol Biol 214:585–595CrossRefPubMedGoogle Scholar
  5. 5.
    Simon M, Metzinger-Le Meuth V, Chevance S, Delalande O, Bondon A (2013) J Biol Inorg Chem 18:27–38CrossRefPubMedGoogle Scholar
  6. 6.
    Lin YW, Wang J (2013) J Inorg Biochem 129:162–171CrossRefPubMedGoogle Scholar
  7. 7.
    Hannibal L, Tomasina F, Capdevila DA, Demicheli V, Tortora V, Alvarez-Paggi D, Jemmerson R, Murgida DH, Radi R (2016) Biochemistry 55:407–428CrossRefPubMedGoogle Scholar
  8. 8.
    Hanske J, Toffey JR, Morenz AM, Bonilla AJ, Schiavoni KH, Pletneva EV (2012) Proc Natl Acad Sci USA 109:125–130CrossRefPubMedGoogle Scholar
  9. 9.
    Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, Amoscato AA, Osipov AN, Belikova NA, Kapralov AA, Kini V, Vlasova II, Zhao Q, Zou M, Di P, Svistunenko DA, Kurnikov IV, Borisenko GG (2005) Nat Chem Biol 1:223–232CrossRefPubMedGoogle Scholar
  10. 10.
    Belikova NA, Vladimirov YA, Osipov AN, Kapralov AA, Tyurin VA, Potapovich MV, Basova LV, Peterson J, Kurnikov IV, Kagan VE (2006) Biochemistry 45:4998–5009CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    McClelland LJ, Mou TC, Jeakins-Cooley ME, Sprang SR, Bowler BE (2014) Proc Natl Acad Sci USA 111:6648–6653CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Rosell FI, Ferrer JC, Mauk AG (1998) J Am Chem Soc 120:11234–11245CrossRefGoogle Scholar
  13. 13.
    Pollock WB, Rosell FI, Twitchett MB, Dumont ME, Mauk AG (1998) Biochemistry 37:6124–6131CrossRefPubMedGoogle Scholar
  14. 14.
    Assfalg M, Bertini I, Dolfi A, Turano P, Mauk AG, Rosell FI, Gray HB (2003) J Am Chem Soc 125:2913–2922CrossRefPubMedGoogle Scholar
  15. 15.
    Assfalg M, Bertini I, Turano P, Mauk AG, Winkler JR, Gray HB (2003) Biophys J 84:3917–3923CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Hirota S, Hattori Y, Nagao S, Taketa M, Komori H, Kamikubo H, Wang Z, Takahashi I, Negi S, Sugiura Y, Kataoka M, Higuchi Y (2010) Proc Natl Acad Sci USA 107:12854–12859CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Bennett MJ, Choe S, Eisenberg D (1994) Proc Natl Acad Sci USA 91:3127–3131CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Liu Y, Eisenberg D (2002) Protein Sci 11:1285–1299CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Rousseau F, Schymkowitz JW, Itzhaki LS (2003) Structure 11:243–251CrossRefPubMedGoogle Scholar
  20. 20.
    Gronenborn AM (2009) Curr Opin Struct Biol 19:39–49CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wang Z, Matsuo T, Nagao S, Hirota S (2011) Org Biomol Chem 9:4766–4769CrossRefPubMedGoogle Scholar
  22. 22.
    Parui PP, Deshpande MS, Nagao S, Kamikubo H, Komori H, Higuchi Y, Kataoka M, Hirota S (2013) Biochemistry 52:8732–8744CrossRefPubMedGoogle Scholar
  23. 23.
    Deshpande MS, Parui PP, Kamikubo H, Yamanaka M, Nagao S, Komori H, Kataoka M, Higuchi Y, Hirota S (2014) Biochemistry 53:4696–4703CrossRefPubMedGoogle Scholar
  24. 24.
    Hayashi Y, Nagao S, Osuka H, Komori H, Higuchi Y, Hirota S (2012) Biochemistry 51:8608–8616CrossRefPubMedGoogle Scholar
  25. 25.
    Nagao S, Ueda M, Osuka H, Komori H, Kamikubo H, Kataoka M, Higuchi Y, Hirota S (2015) PLoS One 10:e0123653CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Ren C, Nagao S, Yamanaka M, Komori H, Shomura Y, Higuchi Y, Hirota S (2015) Mol BioSyst 11:3218–3221CrossRefPubMedGoogle Scholar
  27. 27.
    Miyamoto T, Kuribayashi M, Nagao S, Shomura Y, Higuchi Y, Hirota S (2015) Chem Sci 6:7336–7342CrossRefGoogle Scholar
  28. 28.
    Yamanaka M, Nagao S, Komori H, Higuchi Y, Hirota S (2015) Protein Sci 24:366–375CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Matsuura Y, Takano T, Dickerson RE (1982) J Mol Biol 156:389–409CrossRefPubMedGoogle Scholar
  30. 30.
    Behera RK, Nakajima H, Rajbongshi J, Watanabe Y, Mazumdar S (2013) Biochemistry 52:1373–1384CrossRefPubMedGoogle Scholar
  31. 31.
    Wang ZH, Lin YW, Rosell FI, Ni FY, Lu HJ, Yang PY, Tan XS, Li XY, Huang ZX, Mauk AG (2007) ChemBioChem 8:607–609CrossRefPubMedGoogle Scholar
  32. 32.
    Berry EA, Trumpower BL (1987) Anal Biochem 161:1–15CrossRefPubMedGoogle Scholar
  33. 33.
    Yeh SR, Han SW, Rousseau DL (1998) Accounts Chem Res 31:727–736CrossRefGoogle Scholar
  34. 34.
    Hirota S, Ueda M, Hayashi Y, Nagao S, Kamikubo H, Kataoka M (2012) J Biochem 152:521–529CrossRefPubMedGoogle Scholar
  35. 35.
    Lu Y, Casimiro DR, Bren KL, Richards JH, Gray HB (1993) Proc Natl Acad Sci USA 90:11456–11459CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Silkstone GG, Cooper CE, Svistunenko D, Wilson MT (2005) J Am Chem Soc 127:92–99CrossRefPubMedGoogle Scholar
  37. 37.
    Bren KL, Gray HB, Banci L, Bertini I, Turano P (1995) J Am Chem Soc 117:8067–8073CrossRefGoogle Scholar
  38. 38.
    Banci L, Bertini I, Bren KL, Gray HB, Sompornpisut P, Turano P (1995) Biochemistry 34:11385–11398CrossRefPubMedGoogle Scholar
  39. 39.
    Nugraheni AD, Nagao S, Yanagisawa S, Ogura T, Hirota S (2013) J Biol Inorg Chem 18:383–390CrossRefPubMedGoogle Scholar
  40. 40.
    Brill AS, Williams RJ (1961) Biochem J 78:246–253CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Bennett MJ, Sawaya MR, Eisenberg D (2006) Structure 14:811–824CrossRefPubMedGoogle Scholar
  42. 42.
    Janowski R, Kozak M, Jankowska E, Grzonka Z, Grubb A, Abrahamson M, Jaskolski M (2001) Nat Struct Biol 8:316–320CrossRefPubMedGoogle Scholar
  43. 43.
    Newcomer ME (2002) Curr Opin Struct Biol 12:48–53CrossRefPubMedGoogle Scholar
  44. 44.
    Nurizzo D, Silvestrini MC, Mathieu M, Cutruzzola F, Bourgeois D, Fulop V, Hajdu J, Brunori M, Tegoni M, Cambillau C (1997) Structure 5:1157–1171CrossRefPubMedGoogle Scholar
  45. 45.
    Crane BR, Rosenfeld RJ, Arvai AS, Ghosh DK, Ghosh S, Tainer JA, Stuehr DJ, Getzoff ED (1999) EMBO J 18:6271–6281CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Czjzek M, Létoffé S, Wandersman C, Delepierre M, Lecroisey A, Izadi-Pruneyre N (2007) J Mol Biol 365:1176–1186CrossRefPubMedGoogle Scholar
  47. 47.
    Nagao S, Osuka H, Yamada T, Uni T, Shomura Y, Imai K, Higuchi Y, Hirota S (2012) Dalton Trans 41:11378–11385CrossRefPubMedGoogle Scholar
  48. 48.
    Silva MA, Lucas TG, Salgueiro CA, Gomes CM (2012) PLoS One 7:e46328CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Bai Y, Sosnick TR, Mayne L, Englander SW (1995) Science 269:192–197CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Russell BS, Zhong L, Bigotti MG, Cutruzzola F, Bren KL (2003) J Biol Inorg Chem 8:156–166CrossRefPubMedGoogle Scholar
  51. 51.
    Russell BS, Melenkivitz R, Bren KL (2000) Proc Natl Acad Sci USA 97:8312–8317CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Hong XL, Dixon DW (1989) FEBS Lett 246:105–108CrossRefPubMedGoogle Scholar
  53. 53.
    Yamamoto Y, Terui N, Tachiiri N, Minakawa K, Matsuo H, Kameda T, Hasegawa J, Sambongi Y, Uchiyama S, Kobayashi Y, Igarashi Y (2002) J Am Chem Soc 124:11574–11575CrossRefPubMedGoogle Scholar
  54. 54.
    George P, Glauser SC, Schejter A (1967) J Biol Chem 242:1690–1695PubMedGoogle Scholar

Copyright information

© SBIC 2017

Authors and Affiliations

  • Shun Hirota
    • 1
  • Nobuhiro Yamashiro
    • 1
  • Zhonghua Wang
    • 1
    • 2
  • Satoshi Nagao
    • 1
  1. 1.Graduate School of Materials ScienceNara Institute of Science and TechnologyIkomaJapan
  2. 2.College of Chemistry and Chemical EngineeringChina West Normal UniversityNanchongChina

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