Bacterial cytological profiling rapidly identifies the cellular pathways targeted by antibacterial molecules

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

Volumn 110, Issue 40, 2013, Pages 16169-16174

  Nonejuie, Poochit ^a   Burkart, Michael ^b   Pogliano, Kit ^a   Pogliano, Joe ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antibiotic resistance; Drug screening; High throughput; Pharmacology; Susceptibility

Indexed keywords

ANTIBIOTIC AGENT; SPIROHEXENOLIDE A; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; FUSED HETEROCYCLIC RINGS;

ANTIBIOTIC BIOSYNTHESIS; ARTICLE; CONTROLLED STUDY; CYTOLOGY; DRUG MECHANISM; DRUG TARGETING; INTRACELLULAR SIGNALING; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTON MOTIVE FORCE; DRUG EFFECTS; DRUG SCREENING; EVALUATION STUDY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENETICS; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE; PRINCIPAL COMPONENT ANALYSIS; PROCEDURES; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; CYTOLOGICAL TECHNIQUES; DRUG EVALUATION, PRECLINICAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FLOW CYTOMETRY; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, FLUORESCENCE; PRINCIPAL COMPONENT ANALYSIS; PROTON-MOTIVE FORCE; STAPHYLOCOCCUS AUREUS;

EID: 84885081302     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1311066110     Document Type: Article

References (35)

1. Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336(6086):1268-1273.
2. Hill DA, Artis D (2010) Intestinal bacteria and the regulation of immune cell homeostasis. Annu Rev Immunol 28:623-667.
3. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124(4):837-848.
4. Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489(7415):242-249.
5. Romero D, Traxler MF, López D, Kolter R (2011) Antibiotics as signal molecules. Chem Rev 111(9):5492-5505.
6. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415(6870): 389-395.
7. Nikaido H (2009) Multidrug resistance in bacteria. Annu Rev Biochem 78:119-146.
8. Silver LL (2011) Challenges of antibacterial discovery. Clin Microbiol Rev 24(1):71-109.
9. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL (2007) Drugs for bad bugs: Confronting the challenges of antibacterial discovery. Nat Rev Drug Discov 6(1):29-40.
10. Cotsonas King A, Wu L (2009) Macromolecular synthesis and membrane perturbation assays for mechanisms of action studies of antimicrobial agents. Current Protocols in Pharmacology, eds Enna SJ, et al. (Wiley, Hoboken, NJ).
11. Bandow JE, Hecker M (2007) Proteomic profiling of cellular stresses in Bacillus subtilis reveals cellular networks and assists in elucidating antibiotic mechanisms of action. Systems Biological Approaches in Infectious Diseases, eds Boshoff HI, Barry CE (Birkhäueser, Basel, Switzerland), pp 79-101.
12. Donald RGK, et al. (2009) A Staphylococcus aureus fitness test platform for mechanism-based profiling of antibacterial compounds. Chem Biol 16(8):826-836.
13. Freiberg C, Fischer HP, Brunner NA (2005) Discovering the mechanism of action of novel antibacterial agents through transcriptional profiling of conditional mutants. Antimicrob Agents Chemother 49(2):749-759.
14. Xu HH, Real L, Bailey MW (2006) An array of Escherichia coli clones over-expressing essential proteins: A new strategy of identifying cellular targets of potent antibacterial compounds. Biochem Biophys Res Commun 349(4):1250-1257.
15. Nichols RJ, et al. (2011) Phenotypic landscape of a bacterial cell. Cell 144(1):143-156.
16. Singh SB, Phillips JW, Wang J (2007) Highly sensitive target-based whole-cell antibacterial discovery strategy by antisense RNA silencing. Curr Opin Drug Discov Devel 10(2):160-166.
17. Li X, et al. (2004) Multicopy suppressors for novel antibacterial compounds reveal targets and drug efflux susceptibility. Chem Biol 11(10):1423-1430.
18. Mitchison TJ (2005) Small-molecule screening and profiling by using automated microscopy. ChemBioChem 6(1):33-39.
19. Mayer TU, et al. (1999) Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286(5441):971-974.
20. Lamsa A, Liu WT, Dorrestein PC, Pogliano K (2012) The Bacillus subtilis cannibalism toxin SDP collapses the proton motive force and induces autolysis. Mol Microbiol 84(3):486-500.
21. Jana S, Deb JK (2006) Molecular understanding of aminoglycoside action and resistance. Appl Microbiol Biotechnol 70(2):140-150.
22. Peske F, Savelsbergh A, Katunin VI, Rodnina MV, Wintermeyer W (2004) Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J Mol Biol 343(5):1183-1194.
23. Guan L, Blumenthal RM, Burnham JC (1992) Analysis of macromolecular biosynthesis to define the quinolone-induced postantibiotic effect in Escherichia coli. Antimicrob Agents Chemother 36(10):2118-2124.
24. Menzel TM, et al. (2011) Mode-of-action studies of the novel bisquaternary bisnaphthalimide MT02 against Staphylococcus aureus. Antimicrob Agents Chemother 55(1):311-320.
25. Kang MJ, et al. (2009) Isolation, structure elucidation, and antitumor activity of spirohexenolides A and B. J Org Chem 74(23):9054-9061.
26. Ruiz N, Falcone B, Kahne D, Silhavy TJ (2005) Chemical conditionality: A genetic strategy to probe organelle assembly. Cell 121(2):307-317.
27. Yu W-L, et al. (2013) Spirohexenolide A targets human macrophage migration inhibitory factor (hMIF). J Nat Prod 76(5):817-823.
28. Wiedemann I, et al. (2001) Specific binding of nisin to the peptidoglycan precursor lipid II combines pore formation and inhibition of cell wall biosynthesis for potent antibiotic activity. J Biol Chem 276(3):1772-1779.
29. Bruno ME, Kaiser A, Montville TJ (1992) Depletion of proton motive force by nisin in Listeria monocytogenes cells. Appl Environ Microbiol 58(7):2255-2259.
30. Sims PJ, Waggoner AS, Wang CH, Hoffman JF (1974) Studies on the mechanism by which cyanine dyes measure membrane potential in red blood cells and phosphatidylcholine vesicles. Biochemistry 13(16):3315-3330.
31. Cabrera JE, Cagliero C, Quan S, Squires CL, Jin DJ (2009) Active transcription of rRNA operons condenses the nucleoid in Escherichia coli: Examining the effect of transcription on nucleoid structure in the absence of transertion. J Bacteriol 191(13): 4180-4185.
32. Hud NV, Downing KH (2001) Cryoelectron microscopy of λ phage DNA condensates in vitreous ice: The fine structure of DNA toroids. Proc Natl Acad Sci USA 98(26): 14925-14930.
33. Jin DJ, Cabrera JE (2006) Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli. J Struct Biol 156(2):284-291.
34. Matthew AW (2006) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard. Seventh Edition (CLSI, Wayne, PA), pp 14-18.
35. Pogliano J, et al. (1999) A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Mol Microbiol 31(4):1149-1159.