Tabtoxinine-β-lactam is a "stealth" β-lactam antibiotic that evades β-lactamase-mediated antibiotic resistance

MedChemComm

Volumn 7, Issue 1, 2016, Pages 118-127

  Hart, Kathryn M ^a   Reck, Margaret ^b   Bowman, Gregory R ^a   Wencewicz, Timothy A ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BENZYL PENICILLOIC ACID; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; BETA LACTAMASE CTX M; BETA LACTAMASE CTX M9; BETA LACTAMASE TEM 1; BETA LACTAMASE TEM 64; BETA TABTOXIN BETA LACTAM; CEPHALOSPORIN DERIVATIVE; GLUTAMATE AMMONIA LIGASE; PENICILLIN G; TABTOXININE; TABTOXININE BETA LACTAM; TABTOXININE THREONINE DIPEPTIDE; UNCLASSIFIED DRUG;

ACETYLATION; ADENYLATION; AMP GENE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL STRAIN; BLA GENE; CELL ASSAY; CONTROLLED STUDY; DRUG DETERMINATION; DRUG ISOLATION; DRUG PROTEIN BINDING; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE OVEREXPRESSION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROGEN BOND; HYDROLYSIS; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MEC GENE; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR CLONING; MOLECULAR DOCKING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS SYRINGAE;

EID: 84955307030     PISSN: 20402503     EISSN: 20402511     Source Type: Journal    
DOI: 10.1039/c5md00325c     Document Type: Article

References (52)

1. K. Schwab, in Global Risks 2014, Ninth Edition, Insight Report, World Economic Forum, 2014
2. N. Gupta B. M. Limbago J. B. Patel A. J. Kallen Carbapenem-Resistant Enterobacteriaceae: Epidemiology and Prevention Clin. Infect. Dis. 2011 53 60 67
3. L. E. Nicolle Antimicrobial resistance: The never ending story Can. J. Infect. Dis. 1991 2 47 48
4. C. T. Walsh T. A. Wencewicz Prospects for new antibiotics: a molecule-centered perspective J. Antibiot. 2014 67 7 22
5. D. W. Woolley R. B. Pringle A. C. Braun Isolation of the phytopathogenic toxin of Pseudomonas tabaci, an antagonist of methionine J. Biol. Chem. 1952 197 409 417
6. W. W. Stewart Isolation and proof of structure of wildfire toxin Nature 1971 229 174 178
7. S. L. Sinden R. D. Durbin Glutamine synthetase inhibition: possible mode of action of wildfire toxin from Pseudomonas tabaci Nature 1968 219 379 380
8. M. D. Thomas P. J. Langston-Unkefer T. F. Uchytil R. D. Durbin Inhibition of Glutamine Synthetase from Pea by Tabtoxinine-β-lactam Plant Physiol. 1983 71 912 915
9. P. L. Langston-Unkefer P. A. Macy R. D. Durbin Inactivation of Glutamine Synthetase by Tabtoxinine-β-lactam: Effects of Substrates and pH Plant Physiol. 1984 76 71 74
10. M. A. Fischbach C. T. Walsh Antibiotics for emerging pathogens Science 2009 325 1089 1093
11. K. Bush G. A. Jacoby Updated functional classification of β-lactamases Antimicrob. Agents Chemother. 2010 54 969 976
12. D. R. Bush P. J. Langston-Unkefer Tabtoxinine-β-Lactam Transport into Cultured Corn Cells: Uptake via an Amino Acid Transport System Plant Physiol. 1987 85 845 849
13. T. A. Wencewicz C. T. Walsh Pseudomonas syringae self-protection from tabtoxinine-β-lactam by ligase TblF and acetylase Ttr Biochemistry 2012 51 7712 7725
14. C. T. Knight R. D. Durbin P. J. Langston-Unkefer Role of glutamine synthetase adenylylation in the self-protection of Pseudomonas syringae subsp. "tabaci" from its toxin, tabtoxinine-β-lactam J. Bacteriol. 1986 166 224 229
15. P. J. Kinscherf D. K. Willis The biosynthetic gene cluster for the β-lactam antibiotic tabtoxin in Pseudomonas syringae J. Antibiot. 2005 58 817 821
16. R. H. Coleman J. Shaffer H. True Properties of β-lactamase from Pseudomonas syringae Curr. Microbiol. 1996 32 147 150
17. E. Arrebola F. M. Cazorla A. Perez-Garcia A. Vicente Genes Involved in the Production of Antimetabolite Toxins by Pseudomonas syringae Pathovars Genes 2011 2 640 660
18. P. Y. Savard S. M. Gagne Backbone dynamics of TEM-1 determined by NMR: evidence for a highly ordered protein Biochemistry 2006 45 11414 11424
19. M. Sabate R. Tarrago F. Navarro E. Miro C. Verges J. Barbe G. Prats Cloning and sequence of the gene encoding a novel cefotaxime-hydrolyzing β-lactamase (CTX-M-9) from Escherichia coli in Spain Antimicrob. Agents Chemother. 2000 44 1970 1973
20. X. Wang G. Minasov B. K. Shoichet Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs J. Mol. Biol. 2002 320 85 95
21. M. L. Salverda J. A. De Visser M. Barlow Natural evolution of TEM-1 β-lactamase: experimental reconstruction and clinical relevance FEMS Microbiol. Rev. 2010 34 1015 1036
22. J. Starr M. F. Brown L. Aschenbrenner N. Caspers Y. Che B. S. Gerstenberger M. Huband J. D. Knafels M. M. Lemmon C. Li S. P. McCurdy E. McElroy M. R. Rauckhorst A. P. Tomaras J. A. Young R. P. Zaniewski V. Shanmugasundaram S. Han Siderophore receptor-mediated uptake of lactivicin analogues in gram-negative bacteria J. Med. Chem. 2014 57 3845 3855
23. H. Jeong V. Barbe C. H. Lee D. Vallenet D. S. Yu S. H. Choi A. Couloux S. W. Lee S. H. Yoon L. Cattolico C. G. Hur H. S. Park B. Segurens S. C. Kim T. K. Oh R. E. Lenski F. W. Studier P. Daegelen J. F. Kim Genome sequences of Escherichia coli B strains REL606 and BL21(DE3) J. Mol. Biol. 2009 394 644 652
24. C. Levi R. D. Durbin The isolation and properties of a tabtoxin-hydrolysing aminopeptidase from the periplasm of Pseudomonas syringae pv. tabaci Physiol. Mol. Plant Pathol. 1986 28 345 352
25. P. Swaren L. Maveyraud V. Guillet J. M. Masson L. Mourey J. P. Samama (1995) Electrostatic analysis of TEM1 β-lactamase: effect of substrate binding, steep potential gradients and consequences of site-directed mutations Structure 1993 3 603 613
26. D. C. Marciano N. G. Brown T. Palzkill Analysis of the plasticity of location of the Arg244 positive charge within the active site of the TEM-1 β-lactamase Protein Sci. 2009 18 2080 2089
27. B. P. Atanasov D. Mustafi M. W. Makinen Protonation of the β-lactam nitrogen is the trigger event in the catalytic action of class A β-lactamases Proc. Natl. Acad. Sci. U. S. A. 2000 97 3160 3165
28. A. Matagne J. Lamotte-Brasseur J. M. Frere Interactions between active-site serine β-lactamases and so-called β-lactamase-stable antibiotics. Kinetic and molecular modelling studies Eur. J. Biochem. 1993 217 61 67
29. D. J. Waxman J. L. Strominger Penicillin-binding proteins and the mechanism of action of β-lactam antibiotics Annu. Rev. Biochem. 1983 52 825 869
30. J. A. Kelly O. Dideberg P. Charlier J. P. Wery M. Libert P. C. Moews J. R. Knox C. Duez C. Fraipont B. Joris and et al. On the origin of bacterial resistance to penicillin: comparison of a β-lactamase and a penicillin target Science 1986 231 1429 1431
31. L. Varetto F. De Meester D. Monnaie J. Marchand-Brynaert G. Dive F. Jacob J. M. Frere The importance of the negative charge of β-lactam compounds in the interactions with active-site serine DD-peptidases and β-lactamases Biochem. J. 1991 278 Pt 3 801 807
32. J. Fishovitz J. A. Hermoso M. Chang S. Mobashery Penicillin-binding protein 2a of methicillin-resistant Staphylococcus aureus IUBMB Life 2014 66 572 577
33. M. W. Staude T. E. Frederick S. V. Natarajan B. D. Wilson C. E. Tanner S. T. Ruggiero S. Mobashery J. W. Peng Investigation of signal transduction routes within the sensor/transducer protein BlaR1 of Staphylococcus aureus Biochemistry 2015 54 1600 1610
34. C. Jacobs J. M. Frere S. Normark Cytosolic intermediates for cell wall biosynthesis and degradation control inducible β-lactam resistance in gram-negative bacteria Cell 1997 88 823 832
35. K. Dave T. Palzkill R. F. Pratt Neutral β-Lactams Inactivate High Molecular Mass Penicillin-Binding Proteins of Class B1, Including PBP2a of MRSA ACS Med. Chem. Lett. 2014 5 154 157
36. O. Kocaoglu H. C. Tsui M. E. Winkler E. E. Carlson Profiling of β-lactam selectivity for penicillin-binding proteins in Streptococcus pneumoniae D39 Antimicrob. Agents Chemother. 2015 59 3548 3555
37. Z. Yao D. Kahne R. Kishony Distinct single-cell morphological dynamics under β-lactam antibiotics Mol. Cell 2012 48 705 712
38. K. Poole Resistance to β-lactam antibiotics Cell. Mol. Life Sci. 2004 61 2200 2223
39. S. S. Pao I. T. Paulsen M. H. Saier Major Facilitator Superfamily Microbiol. Mol. Biol. Rev. 1998 62 1 34
40. V. S. Reddy M. A. Shlykov R. Castillo E. I. Sun M. H. Saier Jr. The major facilitator superfamily (MFS) revisited FEBS J. 2012 279 2022 2035
41. A. L. Flores-Mireles J. N. Walker M. Caparon S. J. Hultgren Urinary tract infections: epidemiology, mechanisms of infection and treatment options Nat. Rev. Microbiol. 2015 13 269 284
42. G. Harth M. A. Horwitz An inhibitor of exported Mycobacterium tuberculosis glutamine synthetase selectively blocks the growth of pathogenic mycobacteria in axenic culture and in human monocytes: extracellular proteins as potential novel drug targets J. Exp. Med. 1999 189 1425 1436
43. D. Eisenberg H. S. Gill G. M. Pfluegl S. H. Rotstein Structure-function relationships of glutamine synthetases Biochim. Biophys. Acta 2000 1477 122 145
44. S. L. Mowbray M. K. Kathiravan A. A. Pandey L. R. Odell Inhibition of glutamine synthetase: a potential drug target in Mycobacterium tuberculosis Molecules 2014 19 13161 13176
45. C. Couturier S. Silve R. Morales B. Pessegue S. Llopart A. Nair A. Bauer B. Scheiper C. Pöverlein A. Ganzhorn S. Lagrange E. Bacqué Nanomolar inhibitors of Mycobacterium tuberculosis glutamine synthetase 1: Synthesis, biological evaluation and X-ray crystallographic studies Bioorg. Med. Chem. Lett. 2015 25 1455 1459
46. J. Ghrayeb H. Kimura M. Takahara H. Hsiung Y. Masui M. Inouye Secretion cloning vectors in Escherichia coli EMBO J. 1984 3 2437 2442
47. H. Edelhoch Spectroscopic determination of tryptophan and tyrosine in proteins Biochemistry 1967 6 1948 1954
48. CLSI, in Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard-Ninth Edition, CLSI document M07-A9, Clinical and Laboratory Standards Institute, Wayne, PA, 2012
49. C. H. O'Callaghan A. Morris S. M. Kirby A. H. Shingler Novel method for detection of β-lactamases by using a chromogenic cephalosporin substrate Antimicrob. Agents Chemother. 1972 1 283 288
50. P. C. Hawkins A. G. Skillman G. L. Warren B. A. Ellingson M. T. Stahl Conformer generation with OMEGA: algorithm and validation using high quality structures from the Protein Databank and Cambridge Structural Database J. Chem. Inf. Model. 2010 50 572 584
51. M. McGann FRED pose prediction and virtual screening accuracy J. Chem. Inf. Model. 2011 51 578 596
52. G. A. Jacoby L. S. Munoz-Price The new β-lactamases N. Engl. J. Med. 2005 352 380 391