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

Wang, Fengbin; Singh, Shanteri; Xu, Weijun; Helmich, Kate E.; Miller, Mitchell D.; Cao, Hongnan; Bingman, Craig A.; Thorson, Jon S.; Phillips, George N.

doi:10.1021/acschembio.5b00244

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

Journal Article · Tue Jun 23 00:00:00 EDT 2015 · ACS Chemical Biology

DOI:https://doi.org/10.1021/acschembio.5b00244· OSTI ID:1224012

Wang, Fengbin ^[1]; Singh, Shanteri ^[2]; Xu, Weijun ^[1]; Helmich, Kate E. ^[3]; Miller, Mitchell D. ^[1]; Cao, Hongnan ^[1]; Bingman, Craig A. ^[3]; Thorson, Jon S. ^[2]; Phillips, George N. ^[4]

Rice Univ., Houston, TX (United States)
Univ. of Kentucky, Lexington, KY (United States)
Univ. of Wisconsin, Madison, WI (United States)
Rice Univ., Houston, TX (United States); Univ. of Wisconsin, Madison, WI (United States)

Sugar aminotransferases (SATs) are an important class of tailoring enzymes that catalyze the 5'-pyridoxal phosphate (PLP)-dependent stereo- and regiospecific installation of an amino group from an amino acid donor (typically l-Glu or l-Gln) to a corresponding ketosugar nucleotide acceptor. Herein we report the strategic structural study of two homologous C4 SATs (Micromonospora echinospora CalS13 and Escherichia coli WecE) that utilize identical substrates but differ in their stereochemistry of aminotransfer. This study reveals for the first time a new mode of SAT sugar nucleotide binding and, in conjunction with previously reported SAT structural studies, provides the basis from which to propose a universal model for SAT stereo- and regiochemical control of amine installation. Specifically, the universal model put forth highlights catalytic divergence to derive solely from distinctions within nucleotide sugar orientation upon binding within a relatively fixed SAT active site where the available ligand bound structures of the three out of four representative C3 and C4 SAT examples provide a basis for the overall model. Importantly, this study presents a new predictive model to support SAT functional annotation, biochemical study and rational engineering.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: U01GM098248; UL1TR000117; CA84374

OSTI ID:: 1224012

Journal Information:: ACS Chemical Biology, Vol. 10, Issue 9; ISSN 1554-8929

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 11 works

Citation information provided by
Web of Science

References (41)

Sweet antibiotics – the role of glycosidic residues in antibiotic and antitumor activity and their randomization Křen, Vladimír; Řezanka, Tomáš FEMS Microbiology Reviews, Vol. 32, Issue 5 https://doi.org/10.1111/j.1574-6976.2008.00124.x	journal	August 2008
O-GlcNAc signaling: a metabolic link between diabetes and cancer? Slawson, C.; Copeland, R. J.; Hart, G. W. Trends in Biochemical Sciences, Vol. 35, Issue 10 https://doi.org/10.1016/j.tibs.2010.04.005	journal	October 2010
Enzymatic methods for glyco(diversification/randomization) of drugs and small molecules Gantt, Richard W.; Peltier-Pain, Pauline; Thorson, Jon S. Natural Product Reports, Vol. 28, Issue 11 https://doi.org/10.1039/c1np00045d	journal	January 2011
Carbohydrate-Based Bioactive Compounds for Medicinal Chemistry Applications Cipolla, L.; Peri, F. Mini-Reviews in Medicinal Chemistry, Vol. 11, Issue 1 https://doi.org/10.2174/138955711793564060	journal	January 2011
Glycomics, glycoproteomics and the immune system Kolarich, Daniel; Lepenies, Bernd; Seeberger, Peter H. Current Opinion in Chemical Biology, Vol. 16, Issue 1-2 https://doi.org/10.1016/j.cbpa.2011.12.006	journal	April 2012
Biological Activities of Glucosamine and Its Related Substances Nagaoka, Isao; Igarashi, Mamoru; Sakamoto, Koji Marine Medicinal Foods - Implications and Applications - Animals and Microbes https://doi.org/10.1016/B978-0-12-416003-3.00022-6	book	January 2012
Introduction to glycopathology: the concept, the tools and the perspectives Gabius, Hans-Joachim; Kayser, Klaus Diagnostic Pathology, Vol. 9, Issue 1 https://doi.org/10.1186/1746-1596-9-4	journal	January 2014
The Renaissance of Bacillosamine and Its Derivatives: Pathway Characterization and Implications in Pathogenicity Morrison, Michael J.; Imperiali, Barbara Biochemistry, Vol. 53, Issue 4 https://doi.org/10.1021/bi401546r	journal	January 2014
The sweet spot: defining virus–sialic acid interactions Stencel-Baerenwald, Jennifer E.; Reiss, Kerstin; Reiter, Dirk M. Nature Reviews Microbiology, Vol. 12, Issue 11 https://doi.org/10.1038/nrmicro3346	journal	September 2014
Biosynthesis of deoxyaminosugars in antibiotic-producing bacteria Nedal, A.; Zotchev, S. B. Applied Microbiology and Biotechnology, Vol. 64, Issue 1 https://doi.org/10.1007/s00253-003-1535-9	journal	March 2004
Enzymes of UDP-GlcNAc biosynthesis in yeast Milewski, Sławomir; Gabriel, Iwona; Olchowy, Jarosław Yeast, Vol. 23, Issue 1 https://doi.org/10.1002/yea.1337	journal	January 2006
Increasing carbohydrate diversity via amine oxidation: aminosugar, hydroxyaminosugar, nitrososugar, and nitrosugar biosynthesis in bacteria Timmons, Shannon C.; Thorson, Jon S. Current Opinion in Chemical Biology, Vol. 12, Issue 3 https://doi.org/10.1016/j.cbpa.2008.03.017	journal	June 2008
Natural-Product Sugar Biosynthesis and Enzymatic Glycodiversification Thibodeaux, Christopher J.; Melançon, Charles E.; Liu, Hung-wen Angewandte Chemie International Edition, Vol. 47, Issue 51 https://doi.org/10.1002/anie.200801204	journal	December 2008
Mechanisms and structures of vitamin B6-dependent enzymes involved in deoxy sugar biosynthesis Romo, Anthony J.; Liu, Hung-wen Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1814, Issue 11 https://doi.org/10.1016/j.bbapap.2011.02.003	journal	November 2011
The structural biology of enzymes involved in natural product glycosylation Singh, Shanteri; Phillips Jr., George N.; Thorson, Jon S. Natural Product Reports, Vol. 29, Issue 10 https://doi.org/10.1039/c2np20039b	journal	January 2012
Structural Studies of Salmonella typhimurium ArnB (PmrH) Aminotransferase Noland, Brian W.; Newman, Janet M.; Hendle, Jörg Structure, Vol. 10, Issue 11 https://doi.org/10.1016/S0969-2126(02)00879-1	journal	November 2002
Structural and Functional Characterization of PseC, an Aminotransferase Involved in the Biosynthesis of Pseudaminic Acid, an Essential Flagellar Modification in Helicobacter pylori Schoenhofen, Ian C.; Lunin, Vladimir V.; Julien, Jean-Philippe Journal of Biological Chemistry, Vol. 281, Issue 13 https://doi.org/10.1074/jbc.M512987200	journal	March 2006
Molecular Architecture of DesI: A Key Enzyme in the Biosynthesis of Desosamine ^† ^, ^‡ Burgie, E. Sethe; Holden, Hazel M. Biochemistry, Vol. 46, Issue 31 https://doi.org/10.1021/bi700751d	journal	August 2007
Molecular architecture of DesV fromStreptomyces venezuelae: A PLP-dependent transaminase involved in the biosynthesis of the unusual sugar desosamine Burgie, E. Sethe; Thoden, James B.; Holden, Hazel M. Protein Science, Vol. 16, Issue 5 https://doi.org/10.1110/ps.062711007	journal	May 2007
GDP-Perosamine Synthase: Structural Analysis and Production of a Novel Trideoxysugar ^† ^, ^‡ Cook, Paul D.; Holden, Hazel M. Biochemistry, Vol. 47, Issue 9 https://doi.org/10.1021/bi702430d	journal	March 2008
Structural Analysis of QdtB, an Aminotransferase Required for the Biosynthesis of dTDP-3-acetamido-3,6-dideoxy-α-d-glucose Thoden, James B.; Schäffer, Christina; Messner, Paul Biochemistry, Vol. 48, Issue 7 https://doi.org/10.1021/bi8022015	journal	January 2009
Structural Analysis of WbpE from Pseudomonas aeruginosa PAO1: A Nucleotide Sugar Aminotransferase Involved in O-Antigen Assembly, Larkin, Angelyn; Olivier, Nelson B.; Imperiali, Barbara Biochemistry, Vol. 49, Issue 33 https://doi.org/10.1021/bi100805b	journal	August 2010
The Structure of NtdA, a Sugar Aminotransferase Involved in the Kanosamine Biosynthetic Pathway in Bacillus subtilis, Reveals a New Subclass of Aminotransferases van Straaten, Karin E.; Ko, Jong Bum; Jagdhane, Rajendra Journal of Biological Chemistry, Vol. 288, Issue 47 https://doi.org/10.1074/jbc.M113.500637	journal	November 2013
Structural Basis for Substrate Specificity in ArnB. A Key Enzyme in the Polymyxin Resistance Pathway of Gram-Negative Bacteria Lee, Myeongseon; Sousa, Marcelo C. Biochemistry, Vol. 53, Issue 4 https://doi.org/10.1021/bi4015677	journal	January 2014
Engineering a Methymycin/Pikromycin−Calicheamicin Hybrid: Construction of Two New Macrolides Carrying a Designed Sugar Moiety Zhao, Lishan; Ahlert, Joachim; Xue, Yongquan Journal of the American Chemical Society, Vol. 121, Issue 42 https://doi.org/10.1021/ja992810k	journal	October 1999
The Calicheamicin Gene Cluster and Its Iterative Type I Enediyne PKS Ahlert, J. Science, Vol. 297, Issue 5584 https://doi.org/10.1126/science.1072105	journal	August 2002
Deciphering Indolocarbazole and Enediyne Aminodideoxypentose Biosynthesis through Comparative Genomics: Insights from the AT2433 Biosynthetic Locus Gao, Qunjie; Zhang, Changsheng; Blanchard, Sophie Chemistry & Biology, Vol. 13, Issue 7 https://doi.org/10.1016/j.chembiol.2006.05.009	journal	July 2006
A General NMR-Based Strategy for the in Situ Characterization of Sugar-Nucleotide-Dependent Biosynthetic Pathways Singh, Shanteri; Peltier-Pain, Pauline; Tonelli, Marco Organic Letters, Vol. 16, Issue 12 https://doi.org/10.1021/ol501241a	journal	June 2014
Characterization and Investigation of Substrate Specificity of the Sugar Aminotransferase WecE from E. coli K12 Hwang, Bum-Yeol; Lee, Hwa-Jin; Yang, Yung-Hun Chemistry & Biology, Vol. 11, Issue 7 https://doi.org/10.1016/j.chembiol.2004.04.015	journal	July 2004
Protocols for production of selenomethionine-labeled proteins in 2-L polyethylene terephthalate bottles using auto-induction medium Sreenath, Hassan K.; Bingman, Craig A.; Buchan, Blake W. Protein Expression and Purification, Vol. 40, Issue 2 https://doi.org/10.1016/j.pep.2004.12.022	journal	April 2005
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Characterization of Protein Encoded by spnR from the Spinosyn Gene Cluster of Saccharopolyspora spinosa: Mechanistic Implications for Forosamine Biosynthesis Zhao, Zongbao; Hong, Lin; Liu, Hung-wen Journal of the American Chemical Society, Vol. 127, Issue 21 https://doi.org/10.1021/ja042702k	journal	May 2005
Structural characterization of AtmS13, a putative sugar aminotransferase involved in indolocarbazole AT2433 aminopentose biosynthesis: Structural Characterization of Aminotransferase AtS13 Singh, Shanteri; Kim, Youngchang; Wang, Fengbin Proteins: Structure, Function, and Bioinformatics, Vol. 83, Issue 8 https://doi.org/10.1002/prot.24844	journal	July 2015
Functional characterization and transcriptional analysis of the dnrR1 locus, which controls daunorubicin biosynthesis in Streptomyces peucetius Madduri, K.; Hutchinson, C. R. Journal of Bacteriology, Vol. 177, Issue 5 https://doi.org/10.1128/jb.177.5.1208-1215.1995	journal	March 1995
The entire nogalamycin biosynthetic gene cluster of Streptomyces nogalater: characterization of a 20-kb DNA region and generation of hybrid structures Torkkell, S.; Kunnari, T.; Palmu, K. Molecular Genetics and Genomics, Vol. 266, Issue 2 https://doi.org/10.1007/s004380100554	journal	October 2001
Characterization of mutations in aclacinomycin A-non-producing Streptomyces galilaeus strains with altered glycosylation patterns Räty, Kaj; Hautala, Anne; Torkkell, Sirke Microbiology, Vol. 148, Issue 11 https://doi.org/10.1099/00221287-148-11-3375	journal	November 2002

Cited By (1)

Loop dynamics of thymidine diphosphate-rhamnose 3′-O-methyltransferase (CalS11), an enzyme in calicheamicin biosynthesis Han, Lu; Singh, Shanteri; Thorson, Jon S. Structural Dynamics, Vol. 3, Issue 1 https://doi.org/10.1063/1.4941368	journal	January 2016

Figures / Tables (7)

Similar Records

Structural dynamics of a methionine γ-lyase for calicheamicin biosynthesis: Rotation of the conserved tyrosine stacking with pyridoxal phosphate

Journal Article · Fri Apr 29 00:00:00 EDT 2016 · Structural Dynamics · OSTI ID:1224012

Cao, Hongnan; Tan, Kemin; Wang, Fengbin; +10 more

Structural Analysis of WbpE from Pseudomonas aeruginosa PAO1: A Nucleotide Sugar Aminotransferase Involved in O-Antigen Assembly

Journal Article · Fri Jan 01 00:00:00 EST 2010 · Biochemistry · OSTI ID:1224012

Larkin, A; Olivier, N; Imperiali, B

Structural and Functional Characterization of PseC, an Aminotransferase Involved in the Biosynthesis of Pseudaminic Acid, an Essential Flagellar Modification in Helicobacter Pylori

Journal Article · Sun Jan 01 00:00:00 EST 2006 · J. Biol. Chem. · OSTI ID:1224012

Schoenhofen, I; Lunin, V; Julien, J; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Peptides and proteins
Carbohydrates
Amines
Monomers
Chemical structure