Supramolecular Polymer Formation by a Hemoprotein with a Synthetic Diheme Compound

Overview

Journal FEBS Open Bio

Specialty Biology

Date 2018 Jun 22

PMID 29928574

Authors

Yasuhiro Isogai

Eisuke Takao

Ryuta Nakamura

Minoru Kato

Shigeki Kawabata

Affiliations

Soon will be listed here.

Abstract

Proteins are attractive materials for supramolecular chemistry due to their multifunctionality and self-organization ability. In this work, we synthesized a diheme compound, in which two iron-protoporphyrin IX molecules are associated via a linker chain, and introduced it into a designed four-helix bundle protein with two heme-binding sites. The protein gradually bound the diheme compound by -histidyl ligation and formed supramolecular polymers. Polymer formation was observed by atomic force microscopy (AFM), which revealed the highly branched, dendritic forms of the fibrous architecture. The present results may open a pathway toward nanowire construction with heme-proteins.

References

Baldwin A, Bader R, Christodoulou J, MacPhee C, Dobson C, Barker P . Cytochrome display on amyloid fibrils. J Am Chem Soc. 2006; 128(7):2162-3. DOI: 10.1021/ja0565673. View

Isogai Y, Ota M, Fujisawa T, Izuno H, Mukai M, Nakamura H . Design and synthesis of a globin fold. Biochemistry. 1999; 38(23):7431-43. DOI: 10.1021/bi983006y. View

Koder R, Anderson J, Solomon L, Reddy K, Moser C, Dutton P . Design and engineering of an O(2) transport protein. Nature. 2009; 458(7236):305-9. PMC: 3539743. DOI: 10.1038/nature07841. View

Isogai Y, Ishida M . Design of a novel heme protein with a non-heme globin scaffold. Biochemistry. 2009; 48(34):8136-42. DOI: 10.1021/bi900518q. View

Lopez de la Paz M, Goldie K, Zurdo J, Lacroix E, Dobson C, Hoenger A . De novo designed peptide-based amyloid fibrils. Proc Natl Acad Sci U S A. 2002; 99(25):16052-7. PMC: 138563. DOI: 10.1073/pnas.252340199. View

Gibney B, Rabanal F, Reddy K, Dutton P . Effect of four helix bundle topology on heme binding and redox properties. Biochemistry. 1998; 37(13):4635-43. DOI: 10.1021/bi971856s. View

Robertson D, Farid R, Moser C, Urbauer J, Mulholland S, Pidikiti R . Design and synthesis of multi-haem proteins. Nature. 1994; 368(6470):425-32. DOI: 10.1038/368425a0. View

Bloomer A, Champness J, Bricogne G, Staden R, Klug A . Protein disk of tobacco mosaic virus at 2.8 A resolution showing the interactions within and between subunits. Nature. 2009; 276(5686):362-8. DOI: 10.1038/276362a0. View

Ishida M, Dohmae N, Shiro Y, Oku T, Iizuka T, Isogai Y . Design and synthesis of de novo cytochromes c. Biochemistry. 2004; 43(30):9823-33. DOI: 10.1021/bi049546e. View

10.

Farid T, Kodali G, Solomon L, Lichtenstein B, Sheehan M, Fry B . Elementary tetrahelical protein design for diverse oxidoreductase functions. Nat Chem Biol. 2013; 9(12):826-833. PMC: 4034760. DOI: 10.1038/nchembio.1362. View

11.

Onoda A, Takahashi A, Oohora K, Onuma Y, Hayashi T . Fibrous supramolecular hemoprotein assemblies connected with synthetic heme dimer and apohemoprotein dimer. Chem Biodivers. 2012; 9(9):1684-92. DOI: 10.1002/cbdv.201100434. View

12.

Gibney B, Isogai Y, Rabanal F, Reddy K, Grosset A, Moser C . Self-assembly of heme A and heme B in a designed four-helix bundle: implications for a cytochrome c oxidase maquette. Biochemistry. 2000; 39(36):11041-9. DOI: 10.1021/bi000925r. View

13.

Durbin S, Feher G . Protein crystallization. Annu Rev Phys Chem. 1996; 47:171-204. DOI: 10.1146/annurev.physchem.47.1.171. View

14.

Doll T, Raman S, Dey R, Burkhard P . Nanoscale assemblies and their biomedical applications. J R Soc Interface. 2013; 10(80):20120740. PMC: 3565727. DOI: 10.1098/rsif.2012.0740. View

15.

Kennedy M, Gibney B . Metalloprotein and redox protein design. Curr Opin Struct Biol. 2001; 11(4):485-90. DOI: 10.1016/s0959-440x(00)00237-2. View

16.

Salgado E, Radford R, Tezcan F . Metal-directed protein self-assembly. Acc Chem Res. 2010; 43(5):661-72. PMC: 2873059. DOI: 10.1021/ar900273t. View

17.

Kitagishi H, Oohora K, Yamaguchi H, Sato H, Matsuo T, Harada A . Supramolecular hemoprotein linear assembly by successive interprotein heme-heme pocket interactions. J Am Chem Soc. 2007; 129(34):10326-7. DOI: 10.1021/ja073295q. View

18.

Degrado W, Summa C, Pavone V, NASTRI F, Lombardi A . De novo design and structural characterization of proteins and metalloproteins. Annu Rev Biochem. 2000; 68:779-819. DOI: 10.1146/annurev.biochem.68.1.779. View

19.

Brunsveld L, Folmer B, Meijer E, Sijbesma R . Supramolecular polymers. Chem Rev. 2001; 101(12):4071-98. DOI: 10.1021/cr990125q. View

20.

Solomon L, Kodali G, Moser C, Dutton P . Engineering the assembly of heme cofactors in man-made proteins. J Am Chem Soc. 2014; 136(8):3192-9. PMC: 3985801. DOI: 10.1021/ja411845f. View