Geometric preferences of crosslinked protein-derived cofactors reveal a high propensity for near-sequence pairs

Proteins: Structure, Function and Genetics

Volumn 59, Issue 1, 2005, Pages 64-71

  Swain, Maria D ^a   Benson, David E ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Computational analysis of protein structure; Cross linking (including S S bonds); Protein design; Protein derived cofactors; Structural bioinformatics

Indexed keywords

CYSTEINE; MUTANT PROTEIN;

AMINO ACID SEQUENCE; DISULFIDE BOND; GEOMETRY; MASS SPECTROMETRY; OXIDATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DATA BANK; REVIEW; SEQUENCE ANALYSIS; STRUCTURAL BIOINFORMATICS;

BASE SEQUENCE; BINDING SITES; COENZYMES; CROSS-LINKING REAGENTS; MUTATION; PROTEINS;

EID: 14744281052     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20403     Document Type: Review

References (62)

1. Ito N, Phillips SEV, Stevens C, Ogel ZB, Mcpherson MJ, Keen JN, Yadav KDS, Knowles PF. Novel thioether bond revealed by a 1.7-Å crystal-structure of galactose-oxidase. Nature 1991;350:87-90.
2. McIntire WS, Wemmer DE, Chistoserdov A, Lidstrom ME. A new cofactor in a prokaryotic enzyme: tryptophan tryptophylquinone as the redox prosthetic group in methylamine dehydrogenase. Science 1991;252:817-824.
3. Okeley NM, van der Donk WA. Novel cofactors via post-translational modifications of enzyme active sites. Chem Biol 2000;7:R159-171.
4. Rogers MS, Dooley DM. Posttranslationally modified tyrosines from galactose oxidase and cytochrome c oxidase. Adv Protein Chem 2001;58:387-436.
5. Whittaker JW. Galactose oxidase. Adv Protein Chem 2002;60:1-49.
6. Klinman J. Commentary - how many ways to craft a cofactor? Proc Natl Acad Sci 2001;98:14766-14768.
7. Davidson VL. Pyrroloquinoline quinone (PQQ) from methanol dehydrogenase and tryptophan tryptophylquinone (TTQ) from methylamine dehydrogenase. Adv Protein Chem 2001;58:95-140.
8. Duine JA, Jongejan JA. Quinoproteins, enzymes with pyrroloquinoline quinone as cofactor. Annu Rev Biochem 1989;58:403-426.
9. Stubbe J, van der Donk WA. Protein radicals in enzyme catalysis. Chem Rev 1998;98:705-762.
10. Rogers M, Baron A, McPherson M, Knowles P, Dooley D. Galactose oxidase pro-sequence cleavage and cofactor assembly are self-processing reactions. J Am Chem Soc 2000;122:990-991.
11. Whittaker MM, Whittaker JW. Cu(I)-dependent biogenesis of the galactose oxidase redox cofactor. J Biol Chem 2003;278:22090-22101.
12. Datta S, Mori Y, Takagi K, Kawaguchi K, Chen Z, Okajima T, Kuroda S, Ikeda T, Kano K, Tanizawa K, Mathews F. Structure of a quinohemoprotein amine dehydrogenase with an uncommon redox cofactor and highly unusual crosslinking. Proc Natl Acad Sci 2001;98:14268-14273.
13. Satoh A, Kim JK, Miyahara I, Devreese B, Vandenberghe I, Hacisalihoglu A, Okajima T, Kuroda S, Adachi O, Duine JA, Van Beeumen J, Tanizawa K, Hirotsu K. Crystal structure of quinohemoprotein amine dehydrogenase from Pseudomonas putida. Identification of a novel quinone cofactor encaged by multiple thioether cross-bridges. J Biol Chem 2002;277:2830-2834.
14. Wang Y, Graichen ME, Liu A, Pearson AR, Wilmot CM, Davidson VL. MauG, a novel diheme protein required for tryptophan tryptophylquinone biogenesis. Biochemistry 2003;42:7318-7325.
15. Pearson AR, De la Mora-Rey T, Graichen ME, Wang Y, Jones LH, Marimanikkupam S, Agger SA, Grimsrud PA, Davidson VL, Wilmot CM. Further insights into quinone cofactor biogenesis: Probing the role of mauG in methylamine dehydrogenase tryptophan tryptophylquinone formation. Biochemistry 2004;43:5494-5502.
16. Vandenberghe I, Kim JK, Devreese B, Hacisalihoglu A, Iwabuki H, Okajima T, Kuroda S, Adachi O, Jongejan JA, Duine JA, Tanizawa K, Van Beeumen J. The covalent structure of the mall subunit from Pseudomonas putida amine dehydrogenase reveals the presence of three novel types of internal cross-linkages, all involving cysteine in a thioether bond. J Biol Chem 2001;276:42923-42931.
17. Buse G, Soulimane T, Dewor M, Meyer HE, Bluggel M. Evidence for a copper-coordinated histidine-tyrosine cross-link in the active site of cytochrome oxidase. Protein Sci 1999;8:985-990.
18. Pearson AR, Jones LH, Higgins L, Ashcroft AE, Wilmot CM, Davidson VL. Understanding quinone cofactor biogenesis in methylamine dehydrogenase through novel cofactor generation. Biochemistry 2003;42:3224-3230.
19. Carpena X, Loprasert S, Mongkolsuk S, Switala J, Loewen PC, Fita I. Catalase-peroxidase KatG of Burkholderia pseudomallei at 1.7 Å resolution. J Mol Biol 2003;327:475-489.
20. Yamada Y, Fujiwara T, Sato T, Igarashi N, Tanaka N. The 2.0 Å crystal structure of catalase-peroxidase from Haloarcula marismortui. Nature Struct Biol 2002;9:691-695.
21. Bhaskar B, Immoos CE, Shimizu H, Sulc F, Farmer PJ, Poulos TL. A novel heme and peroxide-dependent tryptophan-tyrosine cross-link in a mutant of cytochrome c peroxidase. J Mol Biol 2003;328:157-166.
22. Sivaraja M, Goodin DB, Smith M, Hoffman BM. Identification by ENDOR of Trp191 as the free-radical site in cytochrome c peroxidase compound ES. Science 1989;245:738-740.
23. Sofia HJ, G. C, Hetzler BG, Reyes-Spindola JF, Miller NE. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information. Nucleic Acids Res 2001;29:1097-1106.
24. Stubbe J, Nocera DG, Yee CS, Chang MCY. Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem Rev 2003;103:2167-2201.
25. Takagi K, Torimura M, Kawaguchi K, Kano K, Ikeda T. Biochemical and electrochemical characterization of quinohemoprotein amine dehydrogenase from Paracoccus denitrificans. Biochemistry 1999;38:6935-6942.
26. Hellinga HW, Richards FM. Construction of new ligand-binding sites in proteins of known structure .1. Computer-aided modeling of sites with predefined geometry. J Mol Biol 1991;222:763-785.
27. Bravo J, Verdaguer N, Tormo J, Betzel C, Switala J, Loewen PC, Fita I. Crystal structure of catalase HPII from Escherichia coli. Structure 1995;3:491-502.
28. Klabunde T, Eicken C, Sacchettini JC, Krebs B. Crystal structure of a plant catechol oxidase containing a dicopper center. Nature Struct Biol 1998;5:1084-1090.
29. Cuff ME, Miller KI, van Holde KE, Hendrickson WA. Crystal structure of a functional unit from Octopus hemocyanin. J Mol Biol 1998;278:855-870.
30. Ostermeier C, Harrenga A, Ermler U, Michel H. Structure at 2.7 angstrom resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody F-V fragment. Proc Natl Acad Sci 1997;94:10547-10553.
31. Yoshikawa S, Shinzawa-Itoh K, Nakashima R, Yaono R, Yamashita E, Inoue N, Yao M, Fei MJ, Libeu CP, Mizushima T, Yamaguchi H, Tomizaki T, Tsukihara T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 1998;280:1723-1729.
32. Chen L, Doi M, Durley RC, Chistoserdov AY, Lidstrom ME, Davidson VL, Mathews FS. Refined crystal structure of methylamine dehydrogenase from Paracoccus denitrificans at 1.75 Å resolution. J Mol Biol 1998;276:131-149.
33. Baumann C, Brockelmann M, Fugmann B, Steffan B, Steglich W, Sheldrick WS. Pigments of fungi. 62. Haematopodin, an unusual pyrroloquinoline derivative isolated from the fungus Mycenahaehaematopus agaricales. Angew Chemie Int Ed 1993;32:1087-1089.
34. Schonenberger B, Jacobson AE, Brossi A, Streaty R, Klee WA, Flippen-Anderson JL, Gilardi R. Comparison of (-)-eseroline with (+)-eseroline and dihydroseco analogs in antinociceptive assays: confirmation of rubreserine structure by x-ray analysis. J Med Chem 1986;29:2268-2273.
35. Lovell SC, Word JM, Richardson JS, Richardson DC. The penultimate rotamer library. Proteins Struct Funct Gen Bioinfor 2000;40: 389-408.
36. Richardson DC, Richardson JS. 500 Filtered Structures. http://kinemage.biochem.duke.edu/databases/top500.php; 2000.
37. Word JM, Lovell SC, LaBean TH, Taylor HC, Zalis ME, Presley BK, Richardson JS, Richardson DC. Visualizing and quantifying molecular goodness-of-fit: small-probe contact dots with explicit hydrogen atoms. J Mol Biol 1999;285:1711-1733.
38. Murzin AG, Brenner SE, Hubbard T, Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 1995;247:536-540.
39. Kalé L, Skeel R, Bhandarkar M, Brunner R, Gursoy A, Krawetz N, Phillips J, Shinozaki A, Varadarajan K, Schulten K. NAMD2: Greater scalability for parallel molecular dynamics. J Comp Phys 1999;151:283-312.
40. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998;102:3586-3616.
41. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. Procheck - a program to check the stereochemical quality of protein structures. J Appl Cryst 1993;26:283-291.
42. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000;28:235-242.
43. Shrake A, Rupley JA. Environment and exposure to solvent of protein atoms. Lysozyme and insulin. J Mol Biol 1973;79:351-371.
44. Pabo CO, Suchanek EG. Computer-aided model-building strategies for protein design. Biochemistry 1986;25:5987-5991.
45. Petersen MT, Jonson PH, Petersen SB. Amino acid neighbours and detailed conformational analysis of cysteines in proteins. Protein Eng 1999;12:535-548.
46. Mas JM, Aloy P, Marti-Renom MA, Oliva B, de Llorens R, Aviles FX, Querol E. Classification of protein disulphide-bridge topologies. J Comp Aided Design 2001;15:477-487.
47. Kraulis PJ. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Cryst 1991;24:946-950.
48. Woycechowsky KJ, Raines RT. The CXC motif: a functional mimic of protein disulfide isomerase. Biochemistry 2003;42:5387-5394.
49. Goldenberg DP, Frieden RW, Haack JA, Morrison TB. Mutational analysis of a protein-folding pathway. Nature 1989;338:127-132.
50. Lerch K. Primary structure of tyrosinase from Neurospora crassa. II. Complete amino acid sequence and chemical structure of a tripeptide containing an unusual thioether. J Biol Chem 1982;257: 6414-6419.
51. Fishel LA, Farnum MF, Mauro JM, Miller MA, Kraut J, Liu Y, Tan XL, Scholes CP. Compound I radical in site-directed mutants of cytochrome c peroxidase as probed by electron paramagnetic resonance and electron-nuclear double resonance. Biochemistry 1991;30:1986-1996.
52. Zhang H, He S, Mauk AG. Radical formation at Tyr39 and Tyr153 following reaction of yeast cytochrome c peroxidase with hydrogen peroxide. Biochemistry 2002;41:13507-13513.
53. Gibson JF, Ingram DJE. Free radical produced in the reaction of methemoglobin with hydrogen peroxide. Nature 1958;181:1398-1399.
54. Svistunenko DA, Dunne J, Fryer M, Nicholls P, Reeder BJ, Wilson MT, Bigotti MG, Cutruzzola F, Cooper CE. Comparative study of tyrosine radicals in hemoglobin and myoglobins treated with hydrogen peroxide. Biophys J 2002;83:2845-2855.
55. 2 reaction. J Am Chem Soc 1996;118:12236-12237.
56. Minetti M, Pietraforte D, Carbone V, Salzano AM, Scorza G, Marino G. Scavenging of peroxynitrite by oxyhemoglobin and identification of modified globin residues. Biochemistry 2000;39: 6689-6697.
57. Amini F, Denison C, Lin HJ, Kuo L, Kodadek T. Using oxidative crosslinking and proximity labeling to quantitatively characterize protein-protein and protein-peptide complexes. Chem Biol 2003;11: 1115-1127.
58. Hawkins CL, Davies MJ. Generation and propagation of radical reactions on proteins. Biochim Biophys Acta 2001;1504:196-219.
59. Atwood CS, Perry G, Zeng H, Kato Y, Jones WD, Ling KQ, Huang X, Moir RD, Wang D, Sayre LM, Smith MA, Chen SG, Bush AI. Copper mediates dityrosine cross-linking of Alzheimer's amyloid-β. Biochemistry 2004;43:560-568.
60. Nagano S, Huang X, Moir RD, Payton SM, Tanzi RE, Bush AI. Peroxidase activity of cyclooxygenase-2 (COX-2) cross-links β-amyloid (Ab) and benerates Aβ-COX-2 hetero-oligomers that are increased in Alzheimer's disease. J Biol Chem 2004;279:14673-14678.
61. Kurumbail RG, Stevens AM, Gierse JK, McDonald JJ, Stegeman RA, Pak JY, Gildehaus D, Miyashiro JM, Penning TD, Seibert K, Isakson PC, Stallings WC. Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 1996;384: 644-648.
62. Rogge CE, Liu W, Wu G, Wang LH, Kulmacz RJ, Tsai AL. Identification of Tyr504 as an alternative tyrosyl radical site in human prostaglandin H synthase-2. Biochemistry 2004;43:1560-1568.