Advertisement

JBIC Journal of Biological Inorganic Chemistry

, Volume 23, Issue 7, pp 1073–1083 | Cite as

Influence of heme c attachment on heme conformation and potential

  • Jesse G. Kleingardner
  • Benjamin D. Levin
  • Giorgio Zoppellaro
  • K. Kristoffer Andersson
  • Sean J. Elliott
  • Kara L. BrenEmail author
Original Paper
Part of the following topical collections:
  1. Alison Butler: Papers in Celebration of Her 2018 ACS Alfred Bader Award in Bioorganic or Bioinorganic Chemistry

Abstract

Heme c is characterized by its covalent attachment to a polypeptide. The attachment is typically to a CXXCH motif in which the two Cys form thioether bonds with the heme, “X” can be any amino acid other than Cys, and the His serves as a heme axial ligand. Some cytochromes c, however, contain heme attachment motifs with three or four intervening residues in a CX3CH or CX4CH motif. Here, the impacts of these variations in the heme attachment motif on heme ruffling and electronic structure are investigated by spectroscopically characterizing CX3CH and CX4CH variants of Hydrogenobacter thermophilus cytochrome c552. In addition, a novel CXCH variant is studied. 1H and 13C NMR, EPR, and resonance Raman spectra of the protein variants are analyzed to deduce the extent of ruffling using previously reported relationships between these spectral data and heme ruffling. In addition, the reduction potentials of these protein variants are measured using protein film voltammetry. The CXCH and CX4CH variants are found to have enhanced heme ruffling and lower reduction potentials. Implications of these results for the use of these noncanonical motifs in nature, and for the engineering of novel heme peptide structures, are discussed.

Keywords

Heme distortion Heme ruffling Reduction potential Cytochrome c Cytochrome c maturation 

Notes

Acknowledgements

This work is supported by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy, Grant No. DE-FG02-09ER16121.

Supplementary material

775_2018_1603_MOESM1_ESM.pdf (2.3 mb)
Supplementary material 1 (PDF 2308 kb)

References

  1. 1.
    Bowman SEJ, Bren KL (2008) Nat Prod Rep 25:1118–1130CrossRefPubMedCentralGoogle Scholar
  2. 2.
    Einsle O, Messerschmidt A, Stach P, Bourenkov GP, Bartunik HD, Huber R, Kroneck PMH (1999) Nature 400:476–480CrossRefGoogle Scholar
  3. 3.
    Arciero DM, Hooper AB (1994) J Biol Chem 269:11878–11886PubMedGoogle Scholar
  4. 4.
    Shimizu H, Schuller DJ, Lanzilotta WN, Sundaramoorthy M, Arciero DM, Hooper AB, Poulos TL (2001) Biochemistry 40:13483–13490CrossRefGoogle Scholar
  5. 5.
    Wang YT, Graichen ME, Liu AM, Pearson AR, Wilmot CM, Davidson VL (2003) Biochemistry 42:7318–7325CrossRefGoogle Scholar
  6. 6.
    Kagan VE, Tyurin VA, Jiang JF, Tyurina YY, Ritov VB, Amoscato AA, Osipov AN, Belikova NA, Kapralov AA, Kini V, Vlasova II, Zhao Q, Zou MM, Di P, Svistunenko DA, Kurnikov IV, Borisenko GG (2005) Nat Chem Biol 1:223–232CrossRefGoogle Scholar
  7. 7.
    Allen JWA (2011) FEBS J 278:4198–4216CrossRefGoogle Scholar
  8. 8.
    Simon J, Hederstedt L (2011) FEBS J 278:4179–4188CrossRefGoogle Scholar
  9. 9.
    Stevens JM, Mavridou DAI, Hamer R, Kritsiligkou P, Goddard AD, Ferguson SJ (2011) FEBS J 278:4170–4178CrossRefPubMedCentralGoogle Scholar
  10. 10.
    Babbitt SE, Sutherland MC, Francisco BS, Mendez DL, Kranz RG (2015) Trends Biochem Sci 40:446–455CrossRefPubMedCentralGoogle Scholar
  11. 11.
    Gabilly ST, Hamel PP (2017) Front Plant Sci 8:1313CrossRefPubMedCentralGoogle Scholar
  12. 12.
    Allen JWA, Barker PD, Daltrop O, Stevens JM, Tomlinson EJ, Sinha N, Sambongi Y, Ferguson SJ (2005) Dalton Trans.  https://doi.org/10.1039/b508139b (ISSN 1477-9226:3410-3418) CrossRefPubMedGoogle Scholar
  13. 13.
    Asher WB, Bren KL (2012) Chem Commun 48:8344–8346CrossRefGoogle Scholar
  14. 14.
    Mavridou DAI, Ferguson SJ, Stevens JM (2013) IUBMB Life 65:209–216CrossRefGoogle Scholar
  15. 15.
    Kleingardner JG, Bren KL (2015) Acc Chem Res 48:1845–1852CrossRefGoogle Scholar
  16. 16.
    Jentzen W, Song XZ, Shelnutt JA (1997) J Phys Chem B 101:1684–1699CrossRefGoogle Scholar
  17. 17.
    Ma JG, Laberge M, Song XZ, Jentzen W, Jia SL, Zhang J, Vanderkooi JM, Shelnutt JA (1998) Biochemistry 37:5118–5128CrossRefGoogle Scholar
  18. 18.
    Shokhireva TK, Berry RE, Uno E, Balfour CA, Zhang HJ, Walker FA (2003) Proc Natl Acad Sci USA 100:3778–3783CrossRefGoogle Scholar
  19. 19.
    Michel LV, Ye T, Bowman SEJ, Levin BD, Hahn MA, Russell BS, Elliott SJ, Bren KL (2007) Biochemistry 46:11753–11760CrossRefPubMedCentralGoogle Scholar
  20. 20.
    Liptak MD, Wen X, Bren KL (2010) J Am Chem Soc 132:9753–9763CrossRefPubMedCentralGoogle Scholar
  21. 21.
    Can M, Zoppellaro G, Andersson KK, Bren KL (2011) Inorg Chem 50:12018–12024CrossRefPubMedCentralGoogle Scholar
  22. 22.
    Galinato MGI, Kleingardner JG, Bowman SEJ, Alp EE, Zhao J, Bren KL, Lehnert N (2012) Proc Natl Acad Sci USA 109:8896–8900CrossRefPubMedCentralGoogle Scholar
  23. 23.
    Sun Y, Benabbas A, Zeng W, Kleingardner JG, Bren KL, Champion PM (2014) Proc Natl Acad Sci USA 111:6570–6575CrossRefPubMedCentralGoogle Scholar
  24. 24.
    Galinato MGI, Bowman SEJ, Kleingardner JG, Martin S, Zhao J, Sturhahn W, Alp EE, Bren KL, Lehnert N (2015) Biochemistry 54:1064–1076CrossRefPubMedCentralGoogle Scholar
  25. 25.
    Bren KL (2016) Isr J Chem 56:693–704CrossRefGoogle Scholar
  26. 26.
    Hobbs JD, Shelnutt JA (1995) J Protein Chem 14:19–25CrossRefPubMedCentralGoogle Scholar
  27. 27.
    Ma JG, Zhang J, Franco R, Jia SL, Moura I, Moura JJG, Kroneck PMH, Shelnutt JA (1998) Biochemistry 37:12431–12442CrossRefPubMedCentralGoogle Scholar
  28. 28.
    Travaglini-Allocatelli C, Gianni S, Dubey VK, Borgia A, Di Matteo A, Bonivento D, Cutruzzolà F, Bren KL, Brunori M (2005) J Biol Chem 280:25729–25734CrossRefPubMedCentralGoogle Scholar
  29. 29.
    Cheng RJ, Chen PY, Gau PR, Chen CC, Peng SM (1997) J Am Chem Soc 119:2563–2569CrossRefGoogle Scholar
  30. 30.
    Shelnutt JA, Song XZ, Ma JG, Jia SL, Jentzen W, Medforth CJ (1998) Chem Soc Rev 27:31–41CrossRefGoogle Scholar
  31. 31.
    Jentzen W, Ma JG, Shelnutt JA (1998) Biophys J 74:753–763CrossRefPubMedCentralGoogle Scholar
  32. 32.
    Hasegawa J, Yoshida T, Yamazaki T, Sambongi Y, Yu Y, Igarashi Y, Kodama T, Yamazaki K, Kyogoku Y, Kobayashi Y (1998) Biochemistry 37:9641–9649CrossRefGoogle Scholar
  33. 33.
    Kleingardner JG, Bren KL (2011) Metallomics 3:396–403CrossRefPubMedCentralGoogle Scholar
  34. 34.
    Braun M, Thöny-Meyer L (2004) Proc Natl Acad Sci USA 101:12830–12835CrossRefGoogle Scholar
  35. 35.
    Kleingardner EC, Asher WB, Bren KL (2017) Biochemistry 56:143–148CrossRefGoogle Scholar
  36. 36.
    Kleingardner JG, Kandemir B, Bren KL (2014) J Am Chem Soc 136:4–7CrossRefGoogle Scholar
  37. 37.
    Rivera M, Walker FA (1995) Anal Biochem 230:295–302CrossRefGoogle Scholar
  38. 38.
    Ye T, Kaur R, Wen X, Bren KL, Elliott SJ (2005) Inorg Chem 44:8999–9006CrossRefGoogle Scholar
  39. 39.
    Fourmond V, Hoke K, Heering HA, Baffert C, Leroux F, Bertrand P, Leger C (2009) Bioelectrochemistry 76:141–147CrossRefGoogle Scholar
  40. 40.
    Kleingardner JG, Bowman SEJ, Bren KL (2013) Inorg Chem 52:12933–12946CrossRefGoogle Scholar
  41. 41.
    Bren KL (2007) In: Scott RA, Lukehart CM (eds) Application of physical methods to inorganic and bioinorganic chemistry. Wiley, Chichester, pp 357–384Google Scholar
  42. 42.
    Takayama SJ, Takahashi Y, Mikami S, Irie K, Kawano S, Yamamoto Y, Hemmi H, Kitahara R, Yokoyama S, Akasaka K (2007) Biochemistry 46:9215–9224CrossRefGoogle Scholar
  43. 43.
    Zhong L, Wen X, Rabinowitz TM, Russell BS, Karan EF, Bren KL (2004) Proc Natl Acad Sci USA 101:8637–8642CrossRefGoogle Scholar
  44. 44.
    Bowman SEJ, Bren KL (2010) Inorg Chem 49:7890–7897CrossRefPubMedCentralGoogle Scholar
  45. 45.
    Karan EF, Russell BS, Bren KL (2002) J Biol Inorg Chem 7:260–272CrossRefGoogle Scholar
  46. 46.
    Nakamura M (2006) Coord Chem Rev 250:2271–2294CrossRefGoogle Scholar
  47. 47.
    Shokhireva TK, Shokhirev NV, Berry RE, Zhang HJ, Walker FA (2008) J Biol Inorg Chem 13:941–959CrossRefGoogle Scholar
  48. 48.
    Walker FA (2003) Inorg Chem 42:4526–4544CrossRefGoogle Scholar
  49. 49.
    Bren KL (2015) In: Swart M, Costas M (eds) Spin states in biochemistry and inorganic chemistry: influence on structure and reactivity. Wiley, Chichester, pp 409–434CrossRefGoogle Scholar
  50. 50.
    Shokhirev NV, Walker FA (1998) J Biol Inorg Chem 3:581–594CrossRefGoogle Scholar
  51. 51.
    Hu SZ, Morris IK, Singh JP, Smith KM, Spiro TG (1993) J Am Chem Soc 115:12446–12458CrossRefGoogle Scholar
  52. 52.
    Czernuszewicz RS, Li XY, Spiro TG (1989) J Am Chem Soc 111:7024–7031CrossRefGoogle Scholar
  53. 53.
    Song XZ, Jentzen W, Jia SL, Jaquinod L, Nurco DJ, Medforth CJ, Smith KM, Shelnutt JA (1996) J Am Chem Soc 118:12975–12988CrossRefGoogle Scholar
  54. 54.
    Taylor CPS (1977) Biochim Biophys Acta 491:137–149CrossRefGoogle Scholar
  55. 55.
    Castner TJ Jr (1959) Phys Rev 115:1506–1515CrossRefGoogle Scholar
  56. 56.
    Zoppellaro G, Harbitz E, Kaur R, Ensign AA, Bren KL, Andersson KK (2008) J Am Chem Soc 130:15348–15360CrossRefPubMedCentralGoogle Scholar
  57. 57.
    Zoppellaro G, Bren KL, Ensign AA, Harbitz E, Kaur R, Hersleth H-P, Ryde U, Hederstedt L, Andersson KK (2009) Biopolymers 91:1064–1082CrossRefPubMedCentralGoogle Scholar
  58. 58.
    Can M, Krucinska J, Zoppellaro G, Andersen NH, Wedekind JE, Hersleth H-P, Andersson KK, Bren KL (2013) ChemBioChem 14:1828–1838CrossRefGoogle Scholar
  59. 59.
    La Mar GN, Horrocks WD Jr, Holm RH (eds) (1973) NMR of paramagnetic molecules: principles and applications. Academic, New YorkGoogle Scholar
  60. 60.
    Bertini I, Luchinat C (1986) NMR of paramagnetic molecules in biological systems. Benjamin Cummings, Menlo ParkGoogle Scholar
  61. 61.
    Walker FA (1999) Coord Chem Rev 186:471–534CrossRefGoogle Scholar
  62. 62.
    Graves AB, Graves MT, Liptak MD (2016) J Phys Chem B 120:3844–3853CrossRefPubMedCentralGoogle Scholar
  63. 63.
    Brautigan DL, Feinberg BA, Hoffman BM, Margoliash E, Peisach J, Blumberg WE (1977) J Biol Chem 252:574–582PubMedPubMedCentralGoogle Scholar
  64. 64.
    Yang F, Knipp M, Shokhireva TK, Berry RE, Zhang HJ, Walker FA (2009) J Biol Inorg Chem 14:1077–1095CrossRefPubMedCentralGoogle Scholar
  65. 65.
    Graves AB, Horak EH, Liptak MD (2016) Dalton Trans 45:10058–10067CrossRefPubMedCentralGoogle Scholar
  66. 66.
    Anderson KK, Hobbs JD, Luo LA, Stanley KD, Quirke JME, Shelnutt JA (1993) J Am Chem Soc 115:12346–12352CrossRefGoogle Scholar
  67. 67.
    Barkigia KM, Chantranupong L, Smith KM, Fajer J (1988) J Am Chem Soc 110:7566–7567CrossRefGoogle Scholar
  68. 68.
    Maes EM, Roberts SA, Weichsel A, Montfort WR (2005) Biochemistry 44:12690–12699CrossRefPubMedCentralGoogle Scholar
  69. 69.
    Aragao D, Frazao C, Sieker L, Sheldrick GM, LeGall J, Carrondo MA (2003) Acta Crystallogr Sect D Biol Crystallogr 59:644–653CrossRefGoogle Scholar
  70. 70.
    Devreese B, Brige A, Backers K, Van Driessche G, Meyer TE, Cusanovich MA, Van Beeumen JJ (2000) Arch Biochem Biophys 381:53–60CrossRefGoogle Scholar
  71. 71.
    Berezhna S, Wohlrab H, Champion PM (2003) Biochemistry 42:6149–6158CrossRefGoogle Scholar
  72. 72.
    Marques HM (2007) Dalton Trans 39:4371–4385CrossRefGoogle Scholar
  73. 73.
    Gong C, Shen Y, Chen J, Song Y, Chen S, Song Y, Wang L (2017) Sens Actuators B 239:890–897CrossRefGoogle Scholar
  74. 74.
    Neumann B, Kielb P, Rustam L, Fischer A, Weidinger IM, Wollenberger U (2017) ChemElectroChem 4:913–919CrossRefGoogle Scholar
  75. 75.
    Korri-Youssoufi H, Desbenoit N, Ricoux R, Mahy JP, Lecomte S (2008) Mater Sci Eng C 28:855–860CrossRefGoogle Scholar
  76. 76.
    Ramanavicius A, Kausaite A, Ramanaviciene A (2005) Biosens Bioelectron 20:1962–1967CrossRefGoogle Scholar
  77. 77.
    Ramanavicius A, Ramanaviciene A (2009) Fuel Cells 9:25–36CrossRefGoogle Scholar
  78. 78.
    Ramanavicius A, Kausaite A, Ramanaviciene A (2008) Biosens Bioelectron 24:761–766CrossRefGoogle Scholar

Copyright information

© SBIC 2018

Authors and Affiliations

  • Jesse G. Kleingardner
    • 1
    • 2
  • Benjamin D. Levin
    • 3
  • Giorgio Zoppellaro
    • 4
  • K. Kristoffer Andersson
    • 5
  • Sean J. Elliott
    • 3
  • Kara L. Bren
    • 1
    Email author
  1. 1.Department of ChemistryUniversity of RochesterRochesterUSA
  2. 2.Department of Chemistry and BiochemistryMessiah CollegeMechanicsburgUSA
  3. 3.Department of ChemistryBoston UniversityBostonUSA
  4. 4.Regional Center of Advanced Technologies and MaterialsOlomoucCzech Republic
  5. 5.Department of BiosciencesUniversity of OsloOsloNorway

Personalised recommendations