Advertisement

Mechanisms of iron mineralization in ferritins: one size does not fit all

  • 1123 Accesses

  • 43 Citations

Abstract

Significant progress has been made in recent years toward understanding the processes by which an iron mineral is deposited within members of the ferritin family of 24mer iron storage proteins, enabled by high-resolution structures together with spectroscopic and kinetic studies. These suggest common characteristics that are shared between ferritins, namely, a highly symmetric arrangement of subunits that provides a protein coat around a central cavity in which the mineral is formed, channels through the coat that facilitate ingress and egress of ions, and catalytic sites, called ferroxidase centers, that drive Fe2+ oxidation. They also reveal significant variations in both structure and mechanism amongst ferritins. Here, we describe three general types of structurally distinct ferroxidase center and the mechanisms of mineralization that they are associated with. The highlighted variation leads us to conclude that there is no universal mechanism by which ferritins function, but instead there exists several distinct mechanisms of ferritin iron mineralization.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. 1.

    Lewin A, Moore GR, Le Brun NE (2005) Dalton Trans 3597–3610

  2. 2.

    Liu XF, Theil EC (2005) Acc Chem Res 38:167–175

  3. 3.

    Theil EC, Matzapetakis M, Liu XF (2006) J Biol Inorg Chem 11:803–810

  4. 4.

    Theil EC (2011) Curr Opin Chem Biol 15:304–311

  5. 5.

    Le Brun NE, Thomson AJ, Moore GR (1997) In metal sites in proteins and models. Springer, Berlin, pp 103–138

  6. 6.

    Aitken-Rogers H, Singleton C, Lewin A, Taylor-Gee A, Moore GR, Le Brun NE (2004) J Biol Inorg Chem 9:161–170

  7. 7.

    Ebrahimi HK, Bill E, Hagedoorn PL, Hagen WR (2012) Nat Chem Biol 8:941–948

  8. 8.

    Le Brun NE, Crow A, Murphy MEP, Mauk AG, Moore GR (2010) Biochim Biophys Acta 1800:732–744

  9. 9.

    Tosha T, Ng HL, Bhattasali O, Alber T, Theil EC (2010) J Am Chem Soc 132:14562–14569

  10. 10.

    Levi S, Santambrogio P, Corsi B, Cozzi A, Arosio P (1996) Biochem J 317:467–473

  11. 11.

    Haldar S, Bevers LE, Tosha T, Theil EC (2011) J Biol Chem 286:25620–25627

  12. 12.

    Liu XF, Jin WL, Theil EC (2003) Proc Natl Acad Sci USA 100:3653–3658

  13. 13.

    Masuda T, Goto F, Yoshihara T, Mikami B (2010) J Biol Chem 285:4049–4059

  14. 14.

    Macedo S, Romao CV, Mitchell E, Matias PM, Liu MY, Xavier AV, LeGall J, Teixeira M, Lindley P, Carrondo MA (2003) Nat Struct Biol 10:285–290

  15. 15.

    Chasteen ND, Harrison PM (1999) J Struct Biol 126:182–194

  16. 16.

    Harrison PM, Arosio P (1996) Biochim Biophys Acta 1275:161–203

  17. 17.

    Li C, Hu X, Zhao G (2009) Biochimie 91:230–239

  18. 18.

    Andrews SC (2010) Biochim Biophys Acta 1800:691–705

  19. 19.

    Abdul-Tehrani H, Hudson AJ, Chang YS, Timms AR, Hawkins C, Williams JM, Harrison PM, Guest JR, Andrews SC (1999) J Bacteriol 181:1415–1428

  20. 20.

    Bertini I, Lalli D, Mangani S, Pozzi C, Rosa C, Theil EC, Turano P (2012) J Am Chem Soc 134:6169–6176

  21. 21.

    Lawson DM, Artymiuk PJ, Yewdall SJ, Smith JMA, Livingstone JC, Treffry A, Luzzago A, Levi S, Arosio P, Cesareni G, Thomas CD, Shaw WV, Harrison PM (1991) Nature 349:541–544

  22. 22.

    Le Brun NE, Wilson MT, Andrews SC, Guest JR, Harrison PM, Thomson AJ, Moore GR (1993) FEBS Lett 333:197–202

  23. 23.

    Hamburger AE, West AP, Hamburger ZA, Hamburger P, Bjorkman PJ (2005) J Mol Biol 349:558–569

  24. 24.

    Toussaint L, Bertrand L, Hue L, Crichton RR, Declercq JP (2007) J Mol Biol 365:440–452

  25. 25.

    Chen-Barrett Y, Harrison PM, Treffry A, Quail MA, Arosio P, Santambrogio P, Chasteen ND (1995) Biochemistry 34:7847–7853

  26. 26.

    Hempstead PD, Hudson AJ, Artymiuk PJ, Andrews SC, Banfield MJ, Guest JR, Harrison PM (1994) FEBS Lett 350:258–262

  27. 27.

    Stillman TJ, Hempstead PD, Artymiuk PJ, Andrews SC, Hudson AJ, Treffry A, Guest JR, Harrison PM (2001) J Mol Biol 307:587–603

  28. 28.

    Tatur J, Hagen WR, Matias PM (2007) J Biol Inorg Chem 12:615–630

  29. 29.

    Johnson E, Cascio D, Sawaya MR, Gingery M, Schroder I (2005) Structure 13:637–648

  30. 30.

    Marchetti A, Parker MS, Moccia LP, Lin EO, Arrieta AL, Ribalet F, Murphy MEP, Maldonado MT, Armbrust EV (2009) Nature 457:467–470

  31. 31.

    Pfaffen S, Abdulqadir R, Le Brun NE, Murphy ME (2013) J Biol Chem 288:14917–14925

  32. 32.

    Andrews SC, Le Brun NE, Barynin V, Thomson AJ, Moore GR, Guest JR, Harrison PM (1995) J Biol Chem 270:23268–23274

  33. 33.

    Frolow F, Kalb AJ, Yariv J (1994) Nat Struct Biol 1:453–460

  34. 34.

    Yasmin S, Andrews SC, Moore GR, Le Brun NE (2011) J Biol Chem 286:3473–3483

  35. 35.

    Crow A, Lawson TL, Lewin A, Moore GR, Le Brun NE (2009) J Am Chem Soc 131:6808–6813

  36. 36.

    Swartz L, Kuchinskas M, Li HY, Poulos TL, Lanzilotta WN (2006) Biochemistry 45:4421–4428

  37. 37.

    Weeratunga SK, Lovell S, Yao H, Battaile KP, Fischer CJ, Gee CE, Rivera M (2010) Biochemistry 49:1160–1175

  38. 38.

    Nordlund P, Sjoberg BM, Eklund H (1990) Nature 345:593–598

  39. 39.

    Rosenzweig AC, Frederick CA, Lippard SJ, Nordlund P (1993) Nature 366:537–543

  40. 40.

    Jameson GNL, Jin W, Krebs C, Perreira AS, Tavares P, Liu XF, Theil EC, Huynh BH (2002) Biochemistry 41:13435–13443

  41. 41.

    Zhao GH, Bou-Abdallah F, Arosio P, Levi S, Janus-Chandler C, Chasteen ND (2003) Biochemistry 42:3142–3150

  42. 42.

    Bou-Abdallah F, Papaefthymiou GC, Scheswohl DM, Stanga SD, Arosio P, Chasteen ND (2002) Biochem J 364:57–63

  43. 43.

    Pereira AS, Small W, Krebs C, Tavares P, Edmondson DE, Theil EC, Huynh BH (1998) Biochemistry 37:9871–9876

  44. 44.

    Moenne-Loccoz P, Krebs C, Herlihy K, Edmondson DE, Theil EC, Huynh BH, Loehr TM (1999) Biochemistry 38:5290–5295

  45. 45.

    Bou-Abdallah F, Zhao GH, Mayne HR, Arosio P, Chasteen ND (2005) J Am Chem Soc 127:3885–3893

  46. 46.

    Zhao GH, Su MH, Chasteen ND (2005) J Mol Biol 352:467–477

  47. 47.

    Zhao ZW, Treffry A, Quail MA, Guest JR, Harrison PM (1997) Dalton Trans 3977–3978

  48. 48.

    Treffry A, Zhao Z, Quail MA, Guest JR, Harrison PM (1995) Biochemistry 34:15204–15213

  49. 49.

    Yang XK, Chen-Barrett Y, Arosio P, Chasteen ND (1998) Biochemistry 37:9743–9750

  50. 50.

    Bauminger ER, Harrison PM, Hechel D, Nowik I, Treffry A (1993) Nucl Instr Meth Phys Res B 76:403–404

  51. 51.

    Pereira AS, Tavares P, Lloyd SG, Danger D, Edmondson DE, Theil EC, Huynh BH (1997) Biochemistry 36:7917–7927

  52. 52.

    Waldo GS, Theil EC (1993) Biochemistry 32:13262–13269

  53. 53.

    Turano P, Lalli D, Felli IC, Theil EC, Bertini I (2010) Proc Natl Acad Sci USA 107:545–550

  54. 54.

    Xu B, Chasteen ND (1991) J Biol Chem 266:19965–19970

  55. 55.

    Treffry A, Zhao ZW, Quail MA, Guest JR, Harrison PM (1998) FEBS Lett 432:213–218

  56. 56.

    Bou-Abdallah F, Yang H, Awomolo A, Cooper B, Woodhall MR, Andrews SC, Chasteen ND (2014) Biochemistry 53:483–495

  57. 57.

    Bauminger ER, Treffry A, Quail MA, Zhao ZW, Nowik I, Harrison PM (1999) Biochemistry 38:7791–7802

  58. 58.

    Bauminger ER, Treffry A, Quail MA, Zhao ZW, Nowik I, Harrison PM (2000) Inorg Chim Acta 297:171–180

  59. 59.

    Ebrahimi KH, Hagedoorn PL, Jongejan JA, Hagen WR (2009) J Biol Inorg Chem 14:1265–1274

  60. 60.

    Ebrahimi KH, Hagedoorn PL, Hagen WR (2013) Chembiochem 14:1123–1133

  61. 61.

    Yang X, Le Brun NE, Thomson AJ, Moore CR, Chasteen ND (2000) Biochemistry 39:4915–4923

  62. 62.

    Bou-Abdallah F, Lewin AC, Le Brun NE, Moore GR, Chasteen ND (2002) J Biol Chem 277:37064–37069

  63. 63.

    Baaghil S, Lewin A, Moore GR, Le Brun NE (2003) Biochemistry 42:14047–14056

  64. 64.

    Lawson TL, Crow A, Lewin A, Yasmin S, Moore GR, Le Brun NE (2009) Biochemistry 48:9031–9039

  65. 65.

    Le Brun NE, Andrews SC, Guest JR, Harrison PM, Moore GR, Thomson AJ (1995) Biochem J 312:385–392

  66. 66.

    Watt GD, Frankel RB, Jacobs D, Huang HQ (1992) Biochemistry 31:5672–5679

  67. 67.

    Wong SG, Tom-Yew SAL, Lewin A, Le Brun NE, Moore GR, Murphy MEP, Mauk AG (2009) J Biol Chem 284:18873–18881

  68. 68.

    DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, San Carlos

Download references

Acknowledgments

We thank the UK’s BBSRC for supporting our work on ferritins through Grant BB/I021884/1.

Author information

Correspondence to Nick E. Le Brun.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bradley, J.M., Moore, G.R. & Le Brun, N.E. Mechanisms of iron mineralization in ferritins: one size does not fit all. J Biol Inorg Chem 19, 775–785 (2014) doi:10.1007/s00775-014-1136-3

Download citation

Keywords

  • Iron storage
  • Ferroxidase
  • Iron metabolism
  • Dinuclear iron
  • Mineralization