Antagonism screen for inhibitors of bacterial cell wall biogenesis uncovers an inhibitor of undecaprenyl diphosphate synthase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 35, 2015, Pages 11048-11053

  Farha, Maya A ^a   Czarny, Tomasz L ^a   Myers, Cullen L ^a   Worrall, Liam J ^b   French, Shawn ^a   Conrady, Deborah G ^b   Wang, Yang ^c   Oldfield, Eric ^c   Strynadka, Natalie C J ^b   Brown, Eric D ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Antagonism; Antibacterial; Undecaprenyl phosphate; UppS; Wall teichoic acids

Indexed keywords

ANTIBIOTIC AGENT; CLOMIFENE; PEPTIDOGLYCAN; SYNTHETASE; TEICHOIC ACID; UNCLASSIFIED DRUG; UNDECAPRENYL DIPHOSPHATE SYNTHASE; ANTIINFECTIVE AGENT; ENZYME INHIBITOR; TRANSFERASE; UNDECAPRENYL PYROPHOSPHATE SYNTHETASE;

ARTICLE; BACTERIAL CELL WALL; BIOGENESIS; BIOSYNTHESIS; CATALYSIS; CELL INTERACTION; CONTROLLED STUDY; DRUG ACTIVITY; DRUG ANTAGONISM; DRUG MECHANISM; DRUG SCREENING; ENZYME ANALYSIS; HIGH THROUGHPUT SCREENING; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; ANTAGONISTS AND INHIBITORS; CELL WALL; DRUG EFFECTS; METABOLISM; MICROBIAL SENSITIVITY TEST;

ALKYL AND ARYL TRANSFERASES; ANTI-BACTERIAL AGENTS; CELL WALL; CLOMIPHENE; ENZYME INHIBITORS; MICROBIAL SENSITIVITY TESTS; STAPHYLOCOCCUS AUREUS;

EID: 84940995323     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1511751112     Document Type: Article

References (42)

1. Falconer SB, Czarny TL, Brown ED (2011) Antibiotics as probes of biological complexity. Nat Chem Biol 7(7):415-423.
2. Farha MA, et al. (2013) Inhibition of WTA synthesis blocks the cooperative action of PBPs and sensitizes MRSA to β-lactams. ACS Chem Biol 8(1):226-233.
3. Lehár J, et al. (2007) Chemical combination effects predict connectivity in biological systems. Mol Syst Biol 3:80.
4. Farha MA, Brown ED (2010) Chemical probes of Escherichia coli uncovered through chemical-chemical interaction profiling with compounds of known biological activity. Chem Biol 17(8):852-862.
5. Yeh P, Tschumi AI, Kishony R (2006) Functional classification of drugs by properties of their pairwise interactions. Nat Genet 38(4):489-494.
6. Cokol M, et al. (2011) Systematic exploration of synergistic drug pairs. Mol Syst Biol 7:544.
7. Yeh PJ, Hegreness MJ, Aiden AP, Kishony R (2009) Drug interactions and the evolution of antibiotic resistance. Nat Rev Microbiol 7(6):460-466.
8. Keith CT, Borisy AA, Stockwell BR (2005) Multicomponent therapeutics for networked systems. Nat Rev Drug Discov 4(1):71-78.
9. Bollenbach T, Quan S, Chait R, Kishony R (2009) Nonoptimal microbial response to antibiotics underlies suppressive drug interactions. Cell 139(4):707-718.
10. Cokol M, et al. (2014) Large-scale identification and analysis of suppressive drug interactions. Chem Biol 21(4):541-551.
11. Chait R, Craney A, Kishony R (2007) Antibiotic interactions that select against resistance. Nature 446(7136):668-671.
12. Michel JB, Yeh PJ, Chait R, Moellering RC, Jr, Kishony R (2008) Drug interactions modulate the potential for evolution of resistance. Proc Natl Acad Sci USA 105(39): 14918-14923.
13. Pasquina LW, Santa Maria JP, Walker S (2013) Teichoic acid biosynthesis as an antibiotic target. Curr Opin Microbiol 16(5):531-537.
14. Sewell EW, Brown ED (2014) Taking aim at wall teichoic acid synthesis: New biology and new leads for antibiotics. J Antibiot (Tokyo) 67(1):43-51.
15. D'Elia MA, et al. (2006) Lesions in teichoic acid biosynthesis in Staphylococcus aureus lead to a lethal gain of function in the otherwise dispensable pathway. J Bacteriol 188(12):4183-4189.
16. Campbell J, et al. (2011) Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in Staphylococcus aureus. ACS Chem Biol 6(1):106-116.
17. Swoboda JG, et al. (2009) Discovery of a small molecule that blocks wall teichoic acid biosynthesis in Staphylococcus aureus. ACS Chem Biol 4(10):875-883.
18. Anonymous; Practice Committee of the American Society for Reproductive Medicine (2013) Use of clomiphene citrate in infertile women: A committee opinion. Fertil Steril 100(2):341-348.
19. Homburg R (2005) Clomiphene citrate: End of an era? A mini-review. Hum Reprod 20(8):2043-2051.
20. Berger-Bächi B, Rohrer S (2002) Factors influencing methicillin resistance in staphylococci. Arch Microbiol 178(3):165-171.
21. de Lencastre H, Tomasz A (1994) Reassessment of the number of auxiliary genes essential for expression of high-level methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 38(11):2590-2598.
22. Tan CM, et al. (2012) Restoring methicillin-resistant Staphylococcus aureus susceptibility to β-lactam antibiotics. Sci Transl Med 4(126):126ra35.
23. Zlitni S, Ferruccio LF, Brown ED (2013) Metabolic suppression identifies new antibacterial inhibitors under nutrient limitation. Nat Chem Biol 9(12):796-804.
24. Pelz A, et al. (2005) Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J Biol Chem 280(37):32493-32498.
25. Zhu W, et al. (2013) Antibacterial drug leads targeting isoprenoid biosynthesis. Proc Natl Acad Sci USA 110(1):123-128.
26. Zhu W, et al. (2015) Antibacterial drug leads: DNA and enzyme multitargeting. J Med Chem 58(3):1215-1227.
27. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
28. Bissantz C, Kuhn B, Stahl M (2010) A medicinal chemist's guide to molecular interactions. J Med Chem 53(14):5061-5084.
29. D'Elia MA, Millar KE, Beveridge TJ, Brown ED (2006) Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J Bacteriol 188(23):8313-8316.
30. Watkinson RJ, Hussey H, Baddiley J (1971) Shared lipid phosphate carrier in the biosynthesis of teichoic acid and peptidoglycan. Nat New Biol 229(2):57-59.
31. Babu M, et al. (2011) Genetic interaction maps in Escherichia coli reveal functional crosstalk among cell envelope biogenesis pathways. PLoS Genet 7(11):e1002377.
32. Lehner B, Crombie C, Tischler J, Fortunato A, Fraser AG (2006) Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. Nat Genet 38(8):896-903.
33. Tong AH, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294(5550):2364-2368.
34. Anderson RG, Hussey H, Baddiley J (1972) The mechanism of wall synthesis in bacteria. The organization of enzymes and isoprenoid phosphates in the membrane. Biochem J 127(1):11-25.
35. Mengin-Lecreulx D, Texier L, Rousseau M, van Heijenoort J (1991) The murG gene of Escherichia coli codes for the UDP-N-acetylglucosamine: N-acetylmuramyl-(pentapeptide) pyrophosphoryl-undecaprenol N-acetylglucosamine transferase involved in the membrane steps of peptidoglycan synthesis. J Bacteriol 173(15):4625-4636.
36. D'Elia MA, et al. (2009) Probing teichoic acid genetics with bioactive molecules reveals new interactions among diverse processes in bacterial cell wall biogenesis. Chem Biol 16(5):548-556.
37. Silver LL (2013) Viable screening targets related to the bacterial cell wall. Ann N Y Acad Sci 1277:29-53.
38. Guo RT, et al. (2007) Bisphosphonates target multiple sites in both cis- and transprenyltransferases. Proc Natl Acad Sci USA 104(24):10022-10027.
39. Jahnke W, et al. (2010) Allosteric non-bisphosphonate FPPS inhibitors identified by fragment-based discovery. Nat Chem Biol 6(9):660-666.
40. Athanasellis G, Igglessi-Markopoulou O, Markopoulos J (2010) Tetramic and tetronic acids as scaffolds in bioinorganic and bioorganic chemistry [published online ahead of print May 25, 2010]. Bioinorg Chem Appl, 10.1155/2010/315056.
41. Durrant JD, et al. (2011) Non-bisphosphonate inhibitors of isoprenoid biosynthesis identified via computer-aided drug design. Chem Biol Drug Des 78(3):323-332.
42. Webb MR (1992) A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc Natl Acad Sci USA 89(11):4884-4887.