Antibiotic efficacy is linked to bacterial cellular respiration

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

Volumn 112, Issue 27, 2015, Pages 8173-8180

  Lobritz, Michael A ^a,b,c,d,e   Belenky, Peter ^f   Porter, Caroline B M ^b,c   Gutierrez, Arnaud ^b,c   Yang, Jason H ^b,c   Schwarz, Eric G ^g   Dwyer, Daniel J ^h   Khalil, Ahmad S ^a,g   Collins, James J ^a,b,c,i  

^a HARVARD UNIVERSITY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f BROWN UNIVERSITY   (United States)

^g Boston University   (United States)

^h Bldg 142   (United States)

ⁱ HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

Antibiotics; Cellular respiration; E. Coli; Metabolomics; S. Aureus

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMPICILLIN; ANTIBIOTIC AGENT; CHLORAMPHENICOL; CLINDAMYCIN; CYTOCHROME C OXIDASE; DAPTOMYCIN; ERYTHROMYCIN; GENTAMICIN; LEVOFLOXACIN; LINEZOLID; NORFLOXACIN; RIFAMPICIN; SPECTINOMYCIN; TETRACYCLINE; ANTIINFECTIVE AGENT;

ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; CELL DEATH; CELL RESPIRATION; DRUG ACTIVITY; DRUG EFFICACY; DRUG TARGETING; ELECTRON TRANSPORT; METABOLOME; PHENOTYPE; PRIORITY JOURNAL; SYNTHESIS; TREATMENT OUTCOME; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIOSYNTHESIS; CLASSIFICATION; DRUG EFFECTS; DRUG INTERACTION; ESCHERICHIA COLI; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METABOLOMICS; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; MUTATION; OXYGEN CONSUMPTION; PROCEDURES; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

ADENOSINE TRIPHOSPHATE; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; DRUG INTERACTIONS; ESCHERICHIA COLI; METABOLOME; METABOLOMICS; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MUTATION; OXYGEN CONSUMPTION; STAPHYLOCOCCUS AUREUS;

EID: 84936134088     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1509743112     Document Type: Article

References (56)

1. Pankey GA, Sabath LD (2004) Clinical relevance of bacteriostatic versus bactericidal mechanisms of action in the treatment of Gram-positive bacterial infections. Clin Infect Dis 38(6):864-870.
2. Finberg RW, et al. (2004) The importance of bactericidal drugs: Future directions in infectious disease. Clin Infect Dis 39(9):1314-1320.
3. Chowdhury MH, Tunkel AR (2000) Antibacterial agents in infections of the central nervous system. Infect Dis Clin North Am 14(2):391-408.
4. Archer G, Fekety FR, Jr (1977) Experimental endocarditis due to Pseudomonas aeruginosa. II. Therapy with carbenicillin and gentamicin. J Infect Dis 136(3): 327-335.
5. Carrizosa J, Kaye D (1977) Antibiotic concentrations in serum, serum bactericidal activity, and results of therapy of streptococcal endocarditis in rabbits. Antimicrob Agents Chemother 12(4):479-483.
6. Weinstein MP, et al. (1985) Multicenter collaborative evaluation of a standardized serum bactericidal test as a prognostic indicator in infective endocarditis. Am J Med 78(2):262-269.
7. Weinstein MP, Stratton CW, Hawley HB, Ackley A, Reller LB (1987) Multicenter collaborative evaluation of a standardized serum bactericidal test as a predictor of therapeutic efficacy in acute and chronic osteomyelitis. Am J Med 83(2):218-222.
8. Klastersky J (1986) Concept of empiric therapy with antibiotic combinations: Indications and limits. Am J Med 80(5C):2-12.
9. Ankomah P, Levin BR (2012) Two-drug antimicrobial chemotherapy: A mathematical model and experiments with Mycobacterium marinum. PLoS Pathog 8(1):e1002487.
10. Ankomah P, Johnson PJ, Levin BR (2013) The pharmaco -, population and evolutionary dynamics of multi-drug therapy: Experiments with S. aureus and E. coli and computer simulations. PLoS Pathog 9(4):e1003300.
11. Crumplin GC, Smith JT (1975) Nalidixic acid: An antibacterial paradox. Antimicrob Agents Chemother 8(3):251-261.
12. Deitz WH, Cook TM, Goss WA (1966) Mechanism of action of nalidixic acid on Escherichia coli. 3. Conditions required for lethality. J Bacteriol 91(2):768-773.
13. Winslow DL, Damme J, Dieckman E (1983) Delayed bactericidal activity of beta-lactam antibiotics against Listeria monocytogenes: antagonism of chloramphenicol and rifampin. Antimicrob Agents Chemother 23(4):555-558.
14. Watanakunakorn C, Guerriero JC (1981) Interaction between vancomycin and rifampin against Staphylococcus aureus. Antimicrob Agents Chemother 19(6):1089-1091.
15. Johansen HK, Jensen TG, Dessau RB, Lundgren B, Frimodt-Moller N (2000) Antagonism between penicillin and erythromycin against Streptococcus pneumoniae in vitro and in vivo. J Antimicrob Chemother 46(6):973-980.
16. Weeks JL, Mason EO, Jr, Baker CJ (1981) Antagonism of ampicillin and chloramphenicol for meningeal isolates of group B streptococci. Antimicrob Agents Chemother 20(3):281-285.
17. Rocco V, Overturf G (1982) Chloramphenicol inhibition of the bactericidal effect of ampicillin against Haemophilus influenzae. Antimicrob Agents Chemother 21(2): 349-351.
18. Brown TH, Alford RH (1984) Antagonism by chloramphenicol of broad-spectrum betalactam antibiotics against Klebsiella pneumoniae. Antimicrob Agents Chemother 25(4):405-407.
19. Lepper MH, Dowling HF (1951) Treatment of pneumococcic meningitis with penicillin compared with penicillin plus aureomycin: Studies including observations on an apparent antagonism between penicillin and aureomycin. AMA Arch Intern Med 88(4): 489-494.
20. Mathies AW, Jr, Leedom JM, Ivler D, Wehrle PF, Portnoy B (1967) Antibiotic antagonism in bacterial meningitis. Antimicrob Agents Chemother (Bethesda) 7:218-224.
21. Coyle EA, Cha R, Rybak MJ (2003) Influences of linezolid, penicillin, and clindamycin, alone and in combination, on streptococcal pyrogenic exotoxin a release. Antimicrob Agents Chemother 47(5):1752-1755.
22. Stevens DL, et al. (2007) Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillin-sensitive and methicillin-resistant Staphylococcus aureus. J Infect Dis 195(2):202-211.
23. Stouthamer AH (1973) A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie van Leeuwenhoek 39(3):545-565.
24. Li GW, Burkhardt D, Gross C, Weissman JS (2014) Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157(3): 624-635.
25. Koebmann BJ, Westerhoff HV, Snoep JL, Nilsson D, Jensen PR (2002) The glycolytic flux in Escherichia coli is controlled by the demand for ATP. J Bacteriol 184(14): 3909-3916.
26. Lin X, Kang L, Li H, Peng X (2014) Fluctuation of multiple metabolic pathways is required for Escherichia coli in response to chlortetracycline stress. Mol Biosyst 10(4):901-908.
27. Rittershaus ES, Baek SH, Sassetti CM (2013) The normalcy of dormancy: Common themes in microbial quiescence. Cell Host Microbe 13(6):643-651.
28. Dwyer DJ, Kohanski MA, Hayete B, Collins JJ (2007) Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli. Mol Syst Biol 3:91.
29. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130(5): 797-810.
30. Kohanski MA, Dwyer DJ, Wierzbowski J, Cottarel G, Collins JJ (2008) Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135(4):679-690.
31. Nandakumar M, Nathan C, Rhee KY (2014) Isocitrate lyase mediates broad antibiotic tolerance in Mycobacterium tuberculosis. Nat Commun 5:4306.
32. Baek SH, Li AH, Sassetti CM (2011) Metabolic regulation of mycobacterial growth and antibiotic sensitivity. PLoS Biol 9(5):e1001065.
33. Thomas VC, et al. (2013) A dysfunctional tricarboxylic acid cycle enhances fitness of Staphylococcus epidermidis during β-lactam stress. MBio 4(4):e00437-13.
34. Grant SS, Kaufmann BB, Chand NS, Haseley N, Hung DT (2012) Eradication of bacterial persisters with antibiotic-generated hydroxyl radicals. Proc Natl Acad Sci USA 109(30): 12147-12152.
35. Dwyer DJ, et al. (2014) Antibiotics induce redox-related physiological alterations as part of their lethality. Proc Natl Acad Sci USA 111(20):E2100-E2109.
36. Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC (2012) Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 336(6079): 315-319.
37. Bettenbrock K, et al. (2014) Towards a systems level understanding of the oxygen response of Escherichia coli. Adv Microb Physiol 64:65-114.
38. Silverman JA, Perlmutter NG, Shapiro HM (2003) Correlation of daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus. Antimicrob Agents Chemother 47(8):2538-2544.
39. Portnoy VA, Herrgård MJ, Palsson BO (2008) Aerobic fermentation of D-glucose by an evolved cytochrome oxidase-deficient Escherichia coli strain. Appl Environ Microbiol 74(24):7561-7569.
40. Perlin DS, Latchney LR, Senior AE (1985) Inhibition of Escherichia coli H+-ATPase by venturicidin, oligomycin and ossamycin. Biochim Biophys Acta 807(3):238-244.
41. Brynildsen MP, Winkler JA, Spina CS, MacDonald IC, Collins JJ (2013) Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production. Nat Biotechnol 31(2):160-165.
42. Wilson DN (2014) Ribosome-targeting antibiotics and mechanisms of bacterial resistance. Nat Rev Microbiol 12(1):35-48.
43. Schneider DA, Gaal T, Gourse RL (2002) NTP-sensing by rRNA promoters in Escherichia coli is direct. Proc Natl Acad Sci USA 99(13):8602-8607.
44. Zhang B, et al. (2011) NMR analysis of a stress response metabolic signaling network. J Proteome Res 10(8):3743-3754.
45. Wang JH, et al. (2014) Sigma S-dependent antioxidant defense protects stationaryphase Escherichia coli against the bactericidal antibiotic gentamicin. Antimicrob Agents Chemother 58(10):5964-5975.
46. Cho H, Uehara T, Bernhardt TG (2014) Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery. Cell 159(6):1300-1311.
47. Richardson DJ (2000) Bacterial respiration: A flexible process for a changing environment. Microbiology 146(Pt 3):551-571.
48. Rubin H, et al. (2015) Acinetobacter baumannii OxPhos inhibitors as selective antiinfective agents. Bioorg Med Chem Lett 25(2):378-383.
49. Schurig-Briccio LA, Yano T, Rubin H, Gennis RB (2014) Characterization of the type 2 NADH:menaquinone oxidoreductases from Staphylococcus aureus and the bactericidal action of phenothiazines. Biochim Biophys Acta 1837(7):954-963.
50. Andries K, et al. (2005) A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307(5707):223-227.
51. Koul A, et al. (2007) Diarylquinolines target subunit c of mycobacterial ATP synthase. Nat Chem Biol 3(6):323-324.
52. Koul A, et al. (2014) Delayed bactericidal response of Mycobacterium tuberculosis to bedaquiline involves remodelling of bacterial metabolism. Nat Commun 5:3369.
53. Hards K, et al. (2015) Bactericidal mode of action of bedaquiline. J Antimicrob Chemother, 10.1093/jac/dkv054.
54. Formentini L, Sánchez-Aragó M, Sánchez-Cenizo L, Cuezva JM (2012) The mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response. Mol Cell 45(6):731-742.
55. Eliopoulos GM, et al. (1986) In vitro and in vivo activity of LY 146032, a new cyclic lipopeptide antibiotic. Antimicrob Agents Chemother 30(4):532-535.
56. Shakoury-Elizeh M, et al. (2010) Metabolic response to iron deficiency in Saccharomyces cerevisiae. J Biol Chem 285(19):14823-14833.