Structural Basis for the Stereochemical Control of Amine Installation in Nucleotide Sugar Aminotransferases

ACS Chemical Biology

Volumn 10, Issue 9, 2015, Pages 2048-2056

  Wang, Fengbin ^a   Singh, Shanteri ^c   Xu, Weijun ^a   Helmich, Kate E ^d   Miller, Mitchell D ^a   Cao, Hongnan ^a   Bingman, Craig A ^d   Thorson, Jon S ^c   Phillips, George N ^a,b,d  

^a Department of Biochemistry and Cell Biology ^*  (United States)

^b RICE UNIVERSITY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE; AMINOTRANSFERASE; NUCLEOTIDE; SUGAR AMINOTRANSFERASE; UNCLASSIFIED DRUG; AMINO ACID; ESCHERICHIA COLI PROTEIN; PYRIDOXAL 5 PHOSPHATE; WECE PROTEIN, E COLI;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BIOCHEMICAL ANALYSIS; CARBOXY TERMINAL SEQUENCE; CHEMICAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; ESCHERICHIA COLI; LIGAND BINDING; MICROMONOSPORA; MICROMONOSPORA ECHINOSPORA; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; STEREOCHEMISTRY; BINDING SITE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

AMINES; AMINO ACIDS; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MICROMONOSPORA; MODELS, MOLECULAR; NUCLEOTIDES; PROTEIN CONFORMATION; PYRIDOXAL PHOSPHATE; SUBSTRATE SPECIFICITY; TRANSAMINASES;

EID: 84937737552     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00244     Document Type: Article

References (43)

1. Kren, V. and Rezanka, T. (2008) Sweet antibiotics-the role of glycosidic residues in antibiotic and antitumor activity and their randomization FEMS Microbiol. Rev. 32, 858-889
2. Slawson, C., Copeland, R. J., and Hart, G. W. (2010) O-GlcNAc signaling: A metabolic link between diabetes and cancer? Trends Biochem. Sci. 35, 547-555
3. Gantt, R. W., Peltier-Pain, P., and Thorson, J. S. (2011) Enzymatic methods for glyco(diversification/randomization) of drugs and small molecules Nat. Prod. Rep. 28, 1811-1853
4. Cipolla, L. and Peri, F. (2011) Carbohydrate-based bioactive compounds for medicinal chemistry applications Mini Rev. Med. Chem. 11, 39-54
5. Kolarich, D., Lepenies, B., and Seeberger, P. H. (2012) Glycomics, glycoproteomics and the immune system Curr. Opin. Chem. Biol. 16, 214-220
6. Nagaoka, I., Igarashi, M., and Sakamoto, K. (2012) Biological activities of glucosamine and its related substances Adv. Food Nutr. Res. 65, 337-352
7. Gabius, H. J. and Kayser, K. (2014) Introduction to glycopathology: The concept, the tools and the perspectives Diagn. Pathol. 9, 4
8. Morrison, M. J. and Imperiali, B. (2014) The renaissance of bacillosamine and its derivatives: Pathway characterization and implications in pathogenicity Biochemistry 53, 624-638
9. Stencel-Baerenwald, J. E., Reiss, K., Reiter, D. M., Stehle, T., and Dermody, T. S. (2014) The sweet spot: defining virus-sialic acid interactions Nat. Rev. Microbiol. 12, 739-749
10. Elshahawi, S. I., Shaaban, K. A., Kharel, M. K., and Thorson, J. S. (2015) A comprehensive review of glycosylated bacterial natural products Chem. Soc. Rev. 10.1039/c4cs00426d
11. Nedal, A. and Zotchev, S. B. (2004) Biosynthesis of deoxyaminosugars in antibiotic-producing bacteria Appl. Microbiol. Biotechnol. 64, 7-15
12. Milewski, S., Gabriel, I., and Olchowy, J. (2006) Enzymes of UDP-GlcNAc biosynthesis in yeast Yeast 23, 1-14
13. Flatt, P. M. and Mahmud, T. (2007) Biosynthesis of aminocyclitol-aminoglycoside antibiotics and related compounds Nat. Prod. Rep. 24, 358-392
14. Timmons, S. C. and Thorson, J. S. (2008) Increasing carbohydrate diversity via amine oxidation: Aminosugar, hydroxyaminosugar, nitrososugar, and nitrosugar biosynthesis in bacteria Curr. Opin. Chem. Biol. 12, 297-305
15. Thibodeaux, C. J., Melancon, C. E., 3rd, and Liu, H. W. (2008) Natural-product sugar biosynthesis and enzymatic glycodiversification Angew. Chem. 47, 9814-9859
16. Romo, A. J. and Liu, H. W. (2011) Mechanisms and structures of vitamin B(6)-dependent enzymes involved in deoxy sugar biosynthesis Biochim. Biophys. Acta 1814, 1534-1547
17. Singh, S., Phillips, G. N., Jr., and Thorson, J. S. (2012) The structural biology of enzymes involved in natural product glycosylation Nat. Prod. Rep. 29, 1201-1237
18. Noland, B. W., Newman, J. M., Hendle, J., Badger, J., Christopher, J. A., Tresser, J., Buchanan, M. D., Wright, T. A., Rutter, M. E., Sanderson, W. E., Muller-Dieckmann, H. J., Gajiwala, K. S., and Buchanan, S. G. (2002) Structural studies of Salmonella typhimurium ArnB (PmrH) aminotransferase: A 4-amino-4-deoxy-L-arabinose lipopolysaccharide-modifying enzyme Structure 10, 1569-1580
19. Schoenhofen, I. C., Lunin, V. V., Julien, J. P., Li, Y., Ajamian, E., Matte, A., Cygler, M., Brisson, J. R., Aubry, A., Logan, S. M., Bhatia, S., Wakarchuk, W. W., and Young, N. M. (2006) Structural and functional characterization of PseC, an aminotransferase involved in the biosynthesis of pseudaminic acid, an essential flagellar modification in Helicobacter pylori J. Biol. Chem. 281, 8907-8916
20. Burgie, E. S. and Holden, H. M. (2007) Molecular architecture of DesI: A key enzyme in the biosynthesis of desosamine Biochemistry 46, 8999-9006
21. Burgie, E. S., Thoden, J. B., and Holden, H. M. (2007) Molecular architecture of DesV from Streptomyces venezuelae: A PLP-dependent transaminase involved in the biosynthesis of the unusual sugar desosamine Protein Sci. 16, 887-896
22. Cook, P. D. and Holden, H. M. (2008) GDP-perosamine synthase: Structural analysis and production of a novel trideoxysugar Biochemistry 47, 2833-2840
23. Thoden, J. B., Schaffer, C., Messner, P., and Holden, H. M. (2009) Structural analysis of QdtB, an aminotransferase required for the biosynthesis of dTDP-3-acetamido-3,6-dideoxy-alpha-D-glucose Biochemistry 48, 1553-1561
24. Larkin, A., Olivier, N. B., and Imperiali, B. (2010) Structural analysis of WbpE from Pseudomonas aeruginosa PAO1: A nucleotide sugar aminotransferase involved in O-antigen assembly Biochemistry 49, 7227-7237
25. van Straaten, K. E., Ko, J. B., Jagdhane, R., Anjum, S., Palmer, D. R., and Sanders, D. A. (2013) The structure of NtdA, a sugar aminotransferase involved in the kanosamine biosynthetic pathway in Bacillus subtilis, reveals a new subclass of aminotransferases J. Biol. Chem. 288, 34121-34130
26. Lee, M. and Sousa, M. C. (2014) Structural basis for substrate specificity in ArnB. A key enzyme in the polymyxin resistance pathway of Gram-negative bacteria Biochemistry 53, 796-805
27. Zhao, L. S., Ahlert, J., Xue, Y. Q., Thorson, J. S., Sherman, D. H., and Liu, H. W. (1999) Engineering a methymycin/pikromycin-calicheamicin hybrid: Construction of two new macrolides carrying a designed sugar moiety J. Am. Chem. Soc. 121, 9881-9882
28. Ahlert, J., Shepard, E., Lomovskaya, N., Zazopoulos, E., Staffa, A., Bachmann, B. O., Huang, K., Fonstein, L., Czisny, A., Whitwam, R. E., Farnet, C. M., and Thorson, J. S. (2002) The calicheamicin gene cluster and its iterative type I enediyne PKS Science 297, 1173-1176
29. Gao, Q., Zhang, C., Blanchard, S., and Thorson, J. S. (2006) Deciphering indolocarbazole and enediyne aminodideoxypentose biosynthesis through comparative genomics: Insights from the AT2433 biosynthetic locus Chem. Biol. 13, 733-743
30. Singh, S., Peltier-Pain, P., Tonelli, M., and Thorson, J. S. (2014) A general NMR-based strategy for the in situ characterization of sugar-nucleotide-dependent biosynthetic pathways Org. Lett. 16, 3220-3223
31. Hwang, B. Y., Lee, H. J., Yang, Y. H., Joo, H. S., and Kim, B. G. (2004) Characterization and investigation of substrate specificity of the sugar aminotransferase WecE from E. coli K12 Chem. Biol. 11, 915-925
32. Sreenath, H. K., Bingman, C. A., Buchan, B. W., Seder, K. D., Burns, B. T., Geetha, H. V., Jeon, W. B., Vojtik, F. C., Aceti, D. J., Frederick, R. O., Phillips, G. N., Jr., and Fox, B. G. (2005) Protocols for production of selenomethionine-labeled proteins in 2-L polyethylene terephthalate bottles using auto-induction medium Protein Expr. Purif. 40, 256-267
33. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Method Enzymol. 276, 307-326
34. Kabsch, W. (2010) Xds Acta Crystallogr., D: Biol. Crystallogr. 66, 125-132
35. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., D: Biol. Crystallogr. 66, 213-221
36. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., D: Biol. Crystallogr. 60, 2126-2132
37. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr., D: Biol. Crystallogr. 66, 12-21
38. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797
39. Zhao, Z., Hong, L., and Liu, H. W. (2005) Characterization of protein encoded by spnR from the spinosyn gene cluster of Saccharopolyspora spinosa: Mechanistic implications for forosamine biosynthesis J. Am. Chem. Soc. 27, 7692-7693
40. Singh, S., Kim, Y., Wang, F., Bigelow, L., Endres, M., Kharel, M. K., Babnigg, G., Bingman, C. A., Joachimiak, A., Thorson, J. S., and Phillips, G. N., Jr. (2015) Structural characterization of AtmS13, a putative sugar aminotransferase involved in indolocarbazole AT2433 aminopentose biosynthesis Proteins 10.1002/prot.24844
41. Madduri, K. and Hutchinson, C. R. (1995) Functional characterization and transcriptional analysis of the dnrR1 locus, which controls daunorubicin biosynthesis in Streptomyces peucetius J. Bact eriol. 177, 1208-1215
42. Torkkell, S., Kunnari, T., Palmu, K., Mäntsälä, P., Hakala, J., and Ylihonko, K. (2001) The entire nogalamycin biosynthetic gene cluster of Streptomyces nogalater: characterization of a 20-kb DNA region and generation of hybrid structures Mol. Genet Genomics 266, 276-288
43. Räty, K., Hautala, A., Torkkell, S., Kantola, J., Mäntsälä, P., Hakala, J., and Ylihonko, K. (2002) Characterization of mutations in aclacinomycin A-non-producing Streptomyces galilaeus strains with altered glycosylation patterns Microbiology. 2002 (148) 3375-3384