Rational disruption of the oligomerization of the mini-ferritin E. coli DPS through protein-protein interface mutation

Protein Science

Volumn 20, Issue 11, 2011, Pages 1907-1917

  Zhang, Yu ^a   Fu, Jing ^a   Chee, Sze Y ^a   Ang, Emmiline X W ^a   Orner, Brendan P ^a  

^a Nanyang Technological University   (Singapore)

Author keywords

Alanine shaving; DPS; Ferritin; Nano cage; Self assembly

Indexed keywords

DPS PROTEIN;

ARTICLE; CIRCULAR DICHROISM; GEL PERMEATION CHROMATOGRAPHY; MUTAGENESIS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SUBSTITUTION; AMINO ACIDS; BACTERIAL OUTER MEMBRANE PROTEINS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FERRITINS; MODELS, MOLECULAR; MUTAGENESIS; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT;

EID: 80054744790     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.731     Document Type: Article

References (38)

1. Dosztanyi Z, Chen J, Dunker AK, Simon I, Tompa P (2006) Disorder and sequence repeats in hub proteins and their implications for network evolution. J Proteome Res 5:2985-2995. (Pubitemid 44749217)
2. Orner BP, Ernst JT, Hamilton AD (2001) Toward proteomimetics: terphenyl derivatives as structural and functional mimics of extended regions of an alpha-helix. J Am Chem Soc 123:5382-5383. (Pubitemid 32910693)
3. Fan RL, Chew SW, Cheong VV, Orner BP (2010) Fabrication of gold nanoparticles inside unmodified horse spleen apoferritin. Small 6:1483-1487.
4. Klem MT, Willits D, Solis DJ, Belcher AM, Young M, Douglas T (2005) Bio-inspired synthesis of protein-encapsulated CoPt nanoparticles. Adv Funct Mater 15: 1489-1494. (Pubitemid 41284830)
5. Meldrum FC, Wade VJ, Nimmo DL, Heywood BR, Mann S (1991) Synthesis of inorganic nanophase materials in supramolecular protein cages. Nature 349: 684-687. (Pubitemid 21912135)
6. Uchida M, Klem MT, Allen M, Suci P, Flenniken M, Gillitzer E, Varpness Z, Liepold LO, Young M, Douglas T (2007) Biological containers: protein cages as multifunctional nanoplatforms. Adv Mater 19:1025-1042. (Pubitemid 46947996)
7. Uchida M, Flenniken ML, Allen M, Willits DA, Crowley BE, Brumfield S, Willis AF, Jackiw L, Jutila M, Young MJ, Douglas T (2006) Targeting of cancer cells with ferrimagnetic ferritin cage nanoparticles. J Am Chem Soc 128:16626-16633. (Pubitemid 46032741)
8. Worsdorfer B, Woycechowsky KJ, Hilvert D (2011) Directed evolution of a protein container. Science 331: 589-592.
9. Orner BP, Liu L, Murphy RM, Kiessling LL (2006) Phage display affords peptides that modulate beta-amyloid aggregation. J Am Chem Soc 128:11882-11889. (Pubitemid 44360224)
10. Ren Y, Wong SM, Lim LY (2007) Folic acid-conjugated protein cages of a plant virus: a novel delivery platform for doxorubicin. Bioconjugate Chem 18:836-843. (Pubitemid 47010805)
11. Weiss GA, Watanabe CK, Zhong A, Goddard A, Sidhu SS (2000) Rapid mapping of protein functional epitopes by combinatorial alanine scanning. Proc Natl Acad Sci USA 97:8950-8954. (Pubitemid 30626654)
12. Cunningham BC, Wells JA (1989) High-resolution epitope mapping of hgh-receptor interactions by alanine-scanning mutagenesis. Science 244:1081-1085. (Pubitemid 19152300)
13. Jin L, Wells JA (1994) Dissecting the energetics of an antibody-antigen interface by alanine shaving and molecular grafting. Protein Sci 3:2351-2357.
14. Grant RA, Filman DJ, Finkel SE, Kolter R, Hogle JM (1998) The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat Struct Biol 5: 294-303. (Pubitemid 28164882)
15. Carrondo MA (2003) Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J 22: 1959-1968. (Pubitemid 36565522)
16. Liu XF, Theil EC (2005) Ferritins: dynamic management of biological iron and oxygen chemistry. Accounts Chem Res 38:167-175.
17. Theil EC (2011) Ferritin protein nanocages use ion channels, catalytic sites, and nucleation channels to manage iron/oxygen chemistry. Curr Opin Chem Biol 15:304-311.
18. Fan R, Boyle AL, Cheong VV, Ng SL, Orner BP (2009) A helix swapping study of two protein cages. Biochemistry 48:5623-5630.
19. Zhang Y, Raudah S, Teo H, Teo GWS, Fan RL, Sun XM, Orner BP (2010) Alanine-shaving mutagenesis to determine key interfacial residues governing the assembly of a nano-cage maxi-ferritin. J Biol Chem 285: 12078-12086.
20. Lawson DM, Treffry A, Artymiuk PJ, Harrison PM, Yewdall SJ, Luzzago A, Cesareni G, Levi S, Arosio P (1989) Identification of the ferroxidase centre in ferritin. Febs Lett 254:207-210. (Pubitemid 19217880)
21. Bellapadrona G, Stefanini S, Zamparelli C, Theil EC, Chiancone E (2009) Iron translocation into and out of Listeria innocua Dps and size distribution of the protein- enclosed nanomineral are modulated by the electrostatic gradient at the 3-fold "ferritin-like" pores. J Biol Chem 284:19101-19109.
22. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797. (Pubitemid 47321791)
23. Jencks WP (1981) On the attribution and additivity of binding-energies. Proc Natl Acad Sci USA 78:4046-4050.
24. Kortemme T, Kim DE, Baker D (2004) Computational alanine scanning of protein-protein interfaces. Sci STKE 2004:pl2.
25. Chiancone E, Ceci P (2010) The multifaceted capacity of Dps proteins to combat bacterial stress conditions: detoxification of iron and hydrogen peroxide and DNA binding. Biochim Biophys Acta 1800:798-805.
26. Swift J, Wehbi WA, Kelly BD, Stowell XF, Saven JG, Dmochowski IJ (2006) Design of functional ferritin-like proteins with hydrophobic cavities. J Am Chem Soc 128:6611-6619.
27. Jaenicke R, Rudolph R (1986) Refolding and association of oligomeric proteins. Methods Enzymol 131: 218-250. (Pubitemid 16002204)
28. Chowdhury RP, Vijayabaskar MS, Vishveshwara S, Chatterji D (2008) Molecular mechanism of in vitro oligomerization of Dps from Mycobacterium smegmatis: mutations of the residues identified by interface cluster analysis. Biochemistry 47:11110-11117.
29. Chowdhury RP, Saraswathi R, Chatterji D (2010) Mycobacterial stress regulation: the Dps twin sister defense mechanism and structure-function relationship. IUBMB Life 62:67-77.
30. Grove A, Wilkinson SP (2005) Differential DNA binding and protection by dimeric and dodecameric forms of the ferritin homolog Dps from Deinococcus radiodurans. J Mol Biol 347:495-508. (Pubitemid 40332360)
31. Chiaraluce R, Consalvi V, Cavallo S, Ilari A, Stefanini S, Chiancone E (2000) The unusual dodecameric ferritin from Listeria innocua dissociates below pH 2.0. Eur J Biochem 267:5733-5741.
32. Ceci P, Ilari A, Falvo E, Giangiacomo L, Chiancone E (2005) Reassessment of protein stability, DNA binding, and protection of Mycobacterium smegmatis Dps. J Biol Chem 280:34776-34785. (Pubitemid 41504611)
33. Gupta S, Chatterji D (2003) Bimodal protection of DNA by Mycobacterium smegmatis DNA-binding protein from stationary phase cells. J Biol Chem 278: 5235-5241. (Pubitemid 36801036)
34. Roy S, Saraswathi R, Gupta S, Sekar K, Chatterji D, Vijayan M (2007) Role of N and C-terminal tails in DNA binding and assembly in Dps: structural studies of Mycobacterium smegmatis Dps deletion mutants. J Mol Biol 370:752-767. (Pubitemid 46879776)
35. Roy S, Gupta S, Das S, Sekar K, Chatterji D, Vijayan M (2004) X-ray analysis of Mycobacterium smegmatis Dps and a comparative study involving other Dps and Dps-like molecules. J Mol Bio 339:1103-1113. (Pubitemid 39303252)
36. Zhang Y, Orner BP (2011) Self-Assembly in the ferritin nano-cage protein superfamily. Int J Mol Sci 12: 5406-5421.
37. Baldwin AJ, Knowles TP, Tartaglia GG, Fitzpatrick AW, Devlin GL, Shammas SL, Waudby CA, Mossuto MF, Meehan S, Gras SL, Christodoulou J, Anthony- Cahill SJ, Barker PD, Vendruscolo M, Dobson CM (2011) Metastability of native proteins and the phenomenon of amyloid formation. J Am Chem Soc 133: 14160-14163.
38. Ardejani MS, Li NX, Orner BP (2011) Stabilization of a protein nanocage through the plugging of a proteinprotein interfacial water pocket. Biochemistry 50: 4029-4037.