Cofactor binding and enzymatic activity in an unevolved superfamily of de novo designed 4-helix bundle proteins

Protein Science

Volumn 18, Issue 7, 2009, Pages 1388-1400

  Patel, Shona C ^a,c   Bradley, Luke H ^b,d   Jinadasa, Sayuri P ^b,e   Hecht, Michael H ^b  

^a Princeton University   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

^e New York Presbyterian Morgan Stanley Children's Hospital   (United States)

Author keywords

4 helix bundle; Binary code; Biomolecular evolution; Protein design; Synthetic biology

Indexed keywords

ESCHERICHIA COLI PROTEIN; ESTERASE; HEME; HEMOPROTEIN; HYDROLASE; MYOGLOBIN; PEROXIDASE; SYNTHETIC DNA; TRIACYLGLYCEROL LIPASE;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; COMBINATORIAL LIBRARY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME KINETICS; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; BIOCATALYSIS; COENZYMES; ENZYMES; EVOLUTION, MOLECULAR; HEME; KINETICS; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

ESCHERICHIA COLI;

EID: 67650022871     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.147     Document Type: Article

References (58)

1. Jensen RA (1976) Enzyme recruitment in evolution of new function. Ann Rev Microbiol 30:409-425.
2. Mandecki W (1990) A method for construction of long randomized open reading frames and polypeptides. Protein Eng 3:221-226.
3. Davidson AR, Sauer RT (1994) Folded proteins occur frequently in libraries of random amino acid sequences. Proc Natl Acad Sci USA 91:2146-2150.
4. Keefe AD, Szostak JW (2001) Functional proteins from a random sequence library. Nature 410:715-718.
5. Watters AL, Baker D (2004) Searching for folded proteins in vitro and in silico. Eur J Biochem 271: 1615-1622.
6. Chiarabelli C, Vrijbloed JW, De Lucrezia D, Thomas RM, Stano P, Polticelli F, Ottone T, Papa E, Luisi PL (2006) Investigation of de novo totally random biosequences. Part II: On the folding frequency in a totally random library of de novo proteins obtained by phage display. Chem Biodivers 3:840-859.
7. Go A, Kim S, Baum J, Hecht MH (2008) Structure and dynamics of de novo proteins from a designed superfamily of 4-helix bundles. Protein Sci 17:821-832.
8. Bradley LH, Kleiner RE, Wang AF, Hecht MH, Wood DW (2005) An intein-based genetic selection enables construction of a high-quality library of binary patterned de novo sequences. Protein Eng Des Sel 18:201-207.
9. Kamtekar S, Schiffer JM, Xiong H, Babik JM, Hecht MH (1993) Protein design by binary patterning of polar and nonpolar amino acids. Science 262:1680-1685.
10. Hecht MH, Das A, Go A, Bradley LH, Wei Y (2004) De novo proteins from designed combinatorial libraries. Protein Sci 13:1711-1723.
11. West MW, Wang W, Patterson J, Mancias JD, Beasley JR, Hecht MH (1999) De novo amyloid proteins from designed combinatorial libraries. Proc Natl Acad Sci USA 96:11211-11216.
12. Wei Y, Liu T, Sazinsky SL, Moffet DA, Pelczer I, Hecht MH (2003) Stably folded de novo proteins from a designed combinatorial library. Protein Sci 12:92-102.
13. Kauzmann W (1959) Some factors in the interpretation of protein denaturation. Adv Protein Chem 14:1-63.
14. Johnson BH, Hecht MH (1994) Recombinant proteins can be isolated from E. coli cells by repeated cycles of freezing and thawing. Biotechnology 12:1357-1360.
15. Wei Y, Kim S, Fela D, Baum J, Hecht MH (2003) Solution structure of a de novo protein from a designed combinatorial library. Proc Natl Acad Sci USA 100: 13270-13273.
16. Roy S, Ratnaswamy G, Boice JA, Fairman R, McLendon G, Hecht MH (1997) A protein designed by binary patterning of polar and nonpolar amino acids displays native-like properties. J Am Chem Soc 119:5302-5306.
17. Roy S, Helmer KJ, Hecht MH (1997) Detecting native-like properties in combinatorial libraries of de novo proteins. Fold Des 2:89-92.
18. Roy S, Hecht MH (2000) Cooperative thermal denaturation of proteins designed by binary patterning of polar and nonpolar amino acids. Biochemistry 39:4603-4607.
19. Rojas NR, Kamtekar S, Simons CT, McLean JE, Vogel KM, Spiro TG, Farid RS, Hecht MH (1997) De novo heme proteins from designed combinatorial libraries. Protein Sci 6:2512-2524.
20. Moffet DA, Certain LK, Smith AJ, Kessel AJ, Beckwith KA, Hecht MH (2000) Peroxidase activity in heme proteins derived from a designed combinatorial library. J Am Chem Soc 122:7612-7613.
21. Wei Y, Hecht MH (2004) Enzyme-like proteins from an unselected library of designed amino acid sequences. Protein Eng Des Sel 17:67-75.
22. Platt J (2007) Senior Thesis. NJ: Princeton University.
23. Webb EC (1992) Recommendations of the nomenclature committee of the International union of biochemistry and molecular biology. Enzyme nomenclature. San Diego: Academic Press, p 23.
24. Orengo CA, Michie AD, Jones DT, Swindells MB, Thornton JM (1997) CATH: a hierarchic classification of protein domain structures. Structure 5:1093-1108.
25. Hiner ANP, Hernandez-Ruiz J, Arnao MB, Garcia-Canovas F, Acosta M (1996) A comparative study of the purity, enzyme activity and inactivation by hydrogen peroxide of commercially available horseradish peroxidase isoenyzmes A and C. Biotechnol Bioeng 50:655-662.
26. Wan L, Twitchett MB, Eltis LD, Mauk AG, Smith M (1998) In vitro evolution of horse heart myoglobin to increase peroxidase activity. Proc Natl Acad Sci USA 95: 12825-12831.
27. Witting PK, Mauk AG, Lay PA (2002) Role of tyrosine-103 in myoglobin peroxidase activity: kinetic and steadystate studies on the reaction of wild-type and variant recombinant human myoglobins with H2O2. Biochemistry 41:11495-11503.
28. Carlsen CU, Skovgaard IM, Skibsted LH (2003) Pseudoperoxidase activity of myoglobin: kinetics and mechanism of the peroxidase cycle of myoglobin and H2O2 and 2,2-Azino-bis(3-ethylbenzthiazoline-6-sulfonate) as substrates. J Agric Food Chem 51:5815-5823.
29. Dwyer MA, Looger LL, Hellinga HW (2008) Retraction of "computational design of a biologically active enzyme." Science 319:569.
30. Reedy CJ, Gibney BR (2004) Heme protein assemblies. Chem Rev 104:617-649.
31. Wilson JR, Caruana DJ, Gilardi G (2003) Engineering redox functions in a nucleic acid binding protein. Chem Commun 356-357.
32. Webb EC (1992) Recommendations of the nomenclature committee of the International union of biochemistry and molecular biology. Enzyme nomenclature. San Diego: Academic Press, p 862.
33. Dimitrov JD, Roumenina LT, Doltchinkova VR, Mihaylova NM, Lacroix-Desmazes S, Kaveri SV, Vassilev TL (2007) Antibodies use heme as a cofactor to extend their pathogen elimination activity and to acquire new effector functions. J Biol Chem 282:26696-26706.
34. Choma CT, Lear JD, Nelson MJ, Dutton PL, Robertson DE, DeGrado WF (1994) Design of a heme-binding four-helix bundle. J Am Chem Soc 116:856-865.
35. Robertson DE, Farid RS, Moser CC, Urbauer JL, Mulholland SE, Pidikiti R, Lear JD, Wand AJ, DeGrado WF, Dutton PL (1994) Design and synthesis of multi-haem proteins. Nature 368:425-432.
36. Arnold PA, Shelton WR, Benson DR (1997) Peptide helix induction in a self-assembling hemoprotein model. J Am Chem Soc 119:3181-3182.
37. Huffman DL, Rosenblatt MM, Suslick KS (1998) Synthetic heme-peptide complexes. J Am Chem Soc 120:6183-6184.
38. Gibney BR, Dutton PL (1999) Histidine placement in de novo-designed heme proteins. Protein Sci 8:1888-1898.
39. Rau HK, DeJonge N, Haehnel W (2000) Combinatorial synthesis of four-helix bundle hemoproteins for tuning of cofactor properties. Angew Chem Int Ed 39:250-253.
40. Koder RL, Valentine KG, Cerda J, Noy D, Wand AJ, Dutton PL (2006) Nativelike structure in designed four a-helix bundles driven by buried polar interactions. J Am Chem Soc 128:14450-14451.
41. Adams PA (1990) The peroxidasic activity of the haem octapeptide microperoxidase-8 (MP-8): the kinetic mechanism of the catalytic reduction of H2O2 by MP-8 using 2,2′-azinobis-(3-ethylbenzothiazoline-6-sulphonate) (ABTS) as reducing substrate. J Chem Soc Perkin Trans 2:1407-1414.
42. Tsuruzono M, Obataya I, Ueno A, Mihara H (2003) Design and peroxidase-like activity of 3 alpha-helix hemoproteins. Peptide Sci 2002:367-368.
43. Broo KS, Nilsson H, Nilsson J, Baltzer L (1998) Substrate recognition and saturation kinetics in de novo designed histidine-based four-helix bundle catalysts. J Am Chem Soc 120:10287-10295.
44. Bolon DN, Mayo SL (2001) Enzyme-like proteins by computational design. Proc Natl Acad Sci USA 98: 14274-14279.
45. Yamauchi A, Nakashima T, Tokuriki N, Hosokawa M, Nogami H, Arioka S, Urabe I, Yomo T (2002) Evolvability of random polypeptides through functional selection within a small library. Protein Eng 15:619-626.
46. Kunitake T, Okahata Y (1976) Catalytic hydrolysis by synthetic polymers. Adv Polym Sci 20:159-221.
47. Clouet A, Darbre T, Reymond JL (2006) Combinatorial synthesis, selection, and properties of esterase peptide dendrimers. Biopolymers 84:114-123.
48. Patel SC (2008) PhD Thesis. NJ: Princeton University.
49. O'Loughlin TL, Patrick WM, Matsumura I (2006) Natural history as a predictor of protein evolvability. Protein Eng Des Sel 19:439-442.
50. O'Brien PJ, Herschlag D (1999) Catalytic promiscuity and the evolution of new enzymatic activities. Chem Biol 6: R91-R105.
51. Aharoni A, Gaidukov L, Khersonsky O, Gould SM, Roodveldt C, Tawfik DS (2005) The "evolvability" of promiscuous protein functions. Nat Genet 37:73-76.
52. Axe DD (2004) Estimating the prevalence of protein sequences adopting functional enzyme folds. J Mol Biol 341:1295-1315.
53. Petrounia PP, Arnold FH (2000) Designed evolution of enzymatic properties. Curr Opin Biotechnol 11:325-330.
54. Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315-1317.
55. Roberts RW, Szostak JW (1997) RNA-peptide fusions for the in vitro selection of peptides and proteins. Proc Natl Acad Sci USA 94:12297-12302.
56. Tawfik DS, Griffiths AD (1998) Man-made cell-like compartments for molecular evolution. Nat Biotechnol 16: 652-656.
57. Arnold FH, Georgiou G (2003) Methods in molecular biology - directed enzyme evolution-screening and selection methods. Totowa, NJ: Humana Press, pp 3-84.
58. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.