Prediction of resistance development against drug combinations by collateral responses to component drugs

Science Translational Medicine

Volumn 6, Issue 262, 2014, Pages

  Munck, Christian ^a   Gumpert, Heidi K ^a   Wallin, Annika I Nilsson ^a   Wang, Harris H ^b   Sommer, Morten O A ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; ANTIBIOTIC AGENT; CHLORAMPHENICOL; CIPROFLOXACIN; PIPERACILLIN; TETRACYCLINE; ANTIINFECTIVE AGENT;

ADAPTATION; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIAL STRAIN; BIOENGINEERING; CHEMOTHERAPY; COLLATERAL RESPONSE; CONTROLLED STUDY; CROSS RESISTANCE; DRUG COMBINATION; DRUG DESIGN; DRUG INTERACTION; DRUG RESISTANCE; DRUG RESPONSE; DRUG SENSITIVITY; DRUG STRUCTURE; ESCHERICHIA COLI; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NEOPLASM; NONHUMAN; PREDICTION; TUBERCULOSIS; ADVERSE EFFECTS; ALLELE; ANTIBIOTIC RESISTANCE; CHEMISTRY; DRUG EFFECTS; GENETICS; HUMAN; IC50; MICROBIAL SENSITIVITY TEST; MOLECULAR EVOLUTION; MUTATION; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; ANTI-BACTERIAL AGENTS; DNA MUTATIONAL ANALYSIS; DRUG DESIGN; DRUG INTERACTIONS; DRUG RESISTANCE, BACTERIAL; DRUG THERAPY, COMBINATION; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; HUMANS; INHIBITORY CONCENTRATION 50; MICROBIAL SENSITIVITY TESTS; MUTATION; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84910654894     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3009940     Document Type: Article

References (76)

1. J. Davies, D. Davies, Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74, 417-433 (2010).
2. P. Nordmann, G. Cuzon, T. Naas, The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect. Dis. 9, 228-236 (2009).
3. P. R. Donald, P. D. van Helden, The global burden of tuberculosis-Combating drug resistance in difficult times. N. Engl. J. Med. 360, 2393-2395 (2009).
4. D. A. Mitchison, How drug resistance emerges as a result of poor compliance during short course chemotherapy for tuberculosis. Int. J. Tuberc. Lung Dis. 2, 10-15 (1998).
5. F. Clavel, A. J. Hance, HIV drug resistance. N. Engl. J. Med. 350, 1023-1035 (2004).
6. E. Dunner, W. B. Brown, J. Wallace, The effect of streptomycin with para-amino salicylic acid on the emergence of resistant strains of tubercle bacilli. Dis. Chest 16, 661-666 (1949).
7. F. J. Palella Jr., K. M. Delaney, A. C. Moorman, M. O. Loveless, J. Fuhrer, G. A. Satten, D. J. Aschman, S. D. Holmberg, Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N. Engl. J. Med. 338, 853-860 (1998).
8. M. S. Glickman, C. L. Sawyers, Converting cancer therapies into cures: Lessons from infectious diseases. Cell 148, 1089-1098 (2012).
9. P. D. Tamma, S. E. Cosgrove, L. L. Maragakis, Combination therapy for treatment of infections with Gram-negative bacteria. Clin. Microbiol. Rev. 25, 450-470 (2012).
10. S. R. Bushby, Trimethoprim-sulfamethoxazole: In vitro microbiological aspects. J. Infect. Dis. 128, S442-S462 (1973).
11. G. Cottarel, J. Wierzbowski, Combination drugs, an emerging option for antibacterial therapy. Trends Biotechnol. 25, 547-555 (2007).
12. M. Shahid, F. Sobia, A. Singh, A. Malik, H. M. Khan, D. Jonas, P. M. Hawkey, Beta-lactams and beta-lactamase-inhibitors in current- or potential-clinical practice: A comprehensive update. Crit. Rev. Microbiol. 35, 81-108 (2009).
13. J. P. Torella, R. Chait, R. Kishony, Optimal drug synergy in antimicrobial treatments. PLOS Comput. Biol. 6, e1000796 (2010).
14. R. Chait, A. Craney, R. Kishony, Antibiotic interactions that select against resistance. Nature 446, 668-671 (2007).
15. M. Hegreness, N. Shoresh, D. Damian, D. Hartl, R. Kishony, Accelerated evolution of resistance in multidrug environments. Proc. Natl. Acad. Sci. U.S.A. 105, 13977-13981 (2008).
16. J. B. Michel, P. J. Yeh, R. Chait, R. C. Moellering Jr., R. Kishony, Drug interactions modulate the potential for evolution of resistance. Proc. Natl. Acad. Sci. U.S.A. 105, 14918-14923 (2008).
17. G. Gadamski, D. Ciarka, J. Gressel, S. W. Gawronski, Negative cross-resistance in triazine-resistant biotypes of Echinochloa crus-galli and Conyza canadensis. Weed Science 48, 176-180 (2000).
18. M. Dragosits, V. Mozhayskiy, S. Quinones-Soto, J. Park, I. Tagkopoulos, Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli. Mol. Syst. Biol. 9, 643 (2013).
19. W. Szybalski, V. Bryson, Genetic studies on microbial cross resistance to toxic agents. I. Cross resistance of Escherichia coli to fifteen antibiotics. J. Bacteriol. 64, 489-499 (1952).
20. L. Chao, An unusual interaction between the target of nalidixic acid and novobiocin. Nature 271, 385-386 (1978).
21. C. C. Sanders, W. E. Sanders Jr., R. V. Goering, V. Werner, Selection of multiple antibiotic resistance by quinolones, b-lactams, and aminoglycosides with special reference to cross-resistance between unrelated drug classes. Antimicrob. Agents Chemother. 26, 797-801 (1984).
22. L. Fernández, R. E. Hancock, Adaptive and mutational resistance: Role of porins and efflux pumps in drug resistance. Clin. Microbiol. Rev. 25, 661-681 (2012).
23. F. L. Muller, S. Colla, E. Aquilanti, V. E. Manzo, G. Genovese, J. Lee, D. Eisenson, R. Narurkar, P. Deng, L. Nezi, M. A. Lee, B. Hu, J. Hu, E. Sahin, D. Ong, E. Fletcher-Sananikone, D. Ho, L. Kwong, C. Brennan, Y. A. Wang, L. Chin, R. A. DePinho, Passenger deletions generate therapeutic vulnerabilities in cancer. Nature 488, 337-342 (2012).
24. K. M. Pluchino, M. D. Hall, A. S. Goldsborough, R. Callaghan, M. M. Gottesman, Collateral sensitivity as a strategy against cancer multidrug resistance. Drug Resist. Updat. 15, 98-105 (2012).
25. K. P. Romano, A. Ali, C. Aydin, D. Soumana, A. Ozen, L. M. Deveau, C. Silver, H. Cao, A. Newton, C. J. Petropoulos, W. Huang, C. A. Schiffer, The molecular basis of drug resistance against hepatitis C virus NS3/4A protease inhibitors. PLOS Pathog. 8, e1002832 (2012).
26. J. Gressel, L. A. Segel, Negative cross resistance; a possible key to atrazine resistance management: A call for whole plant data. Z. Naturforsch. 45c, 470-473 (1990).
27. S. G. Deeks, Treatment of antiretroviral-drug-resistant HIV-1 infection. Lancet 362, 2002-2011 (2003).
28. V. Lázár, G. Pal Singh, R. Spohn, I. Nagy, B. Horváth, M. Hrtyan, R. Busa-Fekete, B. Bogos, O. Méhi, B. Csörgo, G. Pósfai, G. Fekete, B. Szappanos, B. Kégl, B. Papp, C. Pál, Bacterial evolution of antibiotic hypersensitivity. Mol. Syst. Biol. 9, 700 (2013).
29. L. Imamovic, M. O. Sommer, Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Sci. Transl. Med. 5, 204ra132 (2013).
30. D. H. Lee, A. M. Feist, C. L. Barrett, B. Ø. Palsson, Cumulative number of cell divisions as a meaningful timescale for adaptive laboratory evolution of Escherichia coli. PLOS One 6, e26172 (2011).
31. D. C. Hooper, J. S. Wolfson, E. Y. Ng, M. N. Swartz, Mechanisms of action of and resistance to ciprofloxacin. Am. J. Med. 82, 12-20 (1987).
32. W. R. Greco, G. Bravo, J. C. Parsons, The search for synergy: A critical review from a response surface perspective. Pharmacol. Rev. 47, 331-385 (1995).
33. M. J. Lee, A. S. Ye, A. K. Gardino, A. M. Heijink, P. K. Sorger, G. MacBeath, M. B. Yaffe, Sequential application of anticancer drugs enhances cell death by rewiring apoptotic signaling networks. Cell 149, 780-794 (2012).
34. R. Pena-Miller, D. Laehnemann, G. Jansen, A. Fuentes-Hernandez, P. Rosenstiel, H. Schulenburg, R. Beardmore, When the most potent combination of antibiotics selects for the greatest bacterial load: The smile-frown transition. PLOS Biol 11, e1001540 (2013).
35. R. R. Ariza, Z. Li, N. Ringstad, B. Demple, Activation of multiple antibiotic resistance and binding of stress-inducible promoters by Escherichia coli Rob protein. J. Bacteriol. 177, 1655-1661 (1995).
36. A. M. George, S. B. Levy, Gene in the major cotransduction gap of the Escherichia coli K-12 linkage map required for the expression of chromosomal resistance to tetracycline and other antibiotics. J. Bacteriol. 155, 541-548 (1983).
37. D. Ma, M. Alberti, C. Lynch, H. Nikaido, J. E. Hearst, The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol. Microbiol. 19, 101-112 (1996).
38. P. F. Miller, L. F. Gambino, M. C. Sulavik, S. J. Gracheck, Genetic relationship between soxRS and mar loci in promoting multiple antibiotic resistance in Escherichia coli. Antimicrob. Agents Chemother. 38, 1773-1779 (1994).
39. H. Okusu, D. Ma, H. Nikaido, AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J. Bacteriol. 178, 306-308 (1996).
40. E. Toprak, A. Veres, J. B. Michel, R. Chait, D. L. Hartl, R. Kishony, Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat. Genet. 44, 101-105 (2011).
41. M. Oethinger, I. Podglajen, W. V. Kern, S. B. Levy, Overexpression of the marA or soxS regulatory gene in clinical topoisomerase mutants of Escherichia coli. Antimicrob. Agents Chemother. 42, 2089-2094 (1998).
42. K. Maneewannakul, S. B. Levy, Identification for mar mutants among quinolone-resistant clinical isolates of Escherichia coli. Antimicrob. Agents Chemother. 40, 1695-1698 (1996).
43. H. Wang, J. L. Dzink-Fox, M. Chen, S. B. Levy, Genetic characterization of highly fluoroquinolone-resistant clinical Escherichia coli strains from China: Role of acrR mutations. Antimicrob. Agents Chemother. 45, 1515-1521 (2001).
44. T. M. Barbosa, S. B. Levy, Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA. J. Bacteriol. 182, 3467-3474 (2000).
45. M. H. Bennik, P. J. Pomposiello, D. F. Thorne, B. Demple, Defining a rob Regulon in Escherichia coli by using transposon mutagenesis. J. Bacteriol. 182, 3794-3801 (2000).
46. P. J. Pomposiello, M. H. Bennik, B. Demple, Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J. Bacteriol. 183, 3890-3902 (2001).
47. R. G. Martin, J. L. Rosner, Genomics of the marA/soxS/rob regulon of Escherichia coli: Identification of directly activated promoters by application of molecular genetics and informatics to microarray data. Mol. Microbiol. 44, 1611-1624 (2002).
48. D. M. Warner, Q. Yang, V. Duval, M. Chen, Y. Xu, S. B. Levy, Involvement of MarR and YedS in carbapenem resistance in a clinical isolate of Escherichia coli from China. Antimicrob. Agents Chemother. 57, 1935-1937 (2013).
49. L. Martínez-Martínez, Extended-spectrum beta-lactamases and the permeability barrier. Clin. Microbiol. Infect. 14 (Suppl. 1), 82-89 (2008).
50. A. V. Vargiu, H. Nikaido, Multidrug binding properties of the AcrB efflux pump characterized by molecular dynamics simulations. Proc. Natl. Acad. Sci. U.S.A. 109, 20637-20642 (2012).
51. T. Norström, J. Lannergård, D. Hughes, Genetic and phenotypic identification of fusidic acid-resistant mutants with the small-colony-variant phenotype in Staphylococcus aureus. Antimicrob. Agents Chemother. 51, 4438-4446 (2007).
52. U. Johanson, D. Hughes, Fusidic acid-resistant mutants define three regions in elongation factor G of Salmonella typhimurium. Gene 143, 55-59 (1994).
53. M. Macvanin, D. Hughes, Hyper-susceptibility of a fusidic acid-resistant mutant of Salmonella to different classes of antibiotics. FEMS Microbiol. Lett. 247, 215-220 (2005).
54. C. L. Cosma, P. N. Danese, J. H. Carlson, T. J. Silhavy, W. B. Snyder, Mutational activation of the Cpx signal transduction pathway of Escherichia coli suppresses the toxicity conferred by certain envelope-associated stresses. Mol. Microbiol. 18, 491-505 (1995).
55. H. J. Busse, C. Wöstmann, E. P. Bakker, The bactericidal action of streptomycin: Membrane permeabilization caused by the insertion of mistranslated proteins into the cytoplasmic membrane of Escherichia coli and subsequent caging of the antibiotic inside the cells due to degradation of these proteins. J. Gen. Microbiol. 138, 551-561 (1992).
56. M. A. Kohanski, D. J. Dwyer, J. Wierzbowski, G. Cottarel, J. J. Collins, Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135, 679-690 (2008).
57. M. Laviña, A. P. Pugsley, F. Moreno, Identification, mapping, cloning and characterization of a gene (sbmA) required for microcin B17 action on Escherichia coli K12. J. Gen. Microbiol. 132, 1685-1693 (1986).
58. R. E. de Cristóbal, P. A. Vincent, R. A. Salomón, A combination of sbmA and tolC mutations in Escherichia coli K-12 Tn10-carrying strains results in hypersusceptibility to tetracycline. J. Bacteriol. 190, 1491-1494 (2008).
59. P. J. Yeh, M. J. Hegreness, A. P. Aiden, R. Kishony, Drug interactions and the evolution of antibiotic resistance. Nat. Rev. Microbiol. 7, 460-466 (2009).
60. N. Frimodt-Møller, How predictive is PK/PD for antibacterial agents?. Int. J. Antimicrob. Agents 19, 333-339 (2002).
61. M. J. Rybak, Pharmacodynamics: Relation to antimicrobial resistance. Am. J. Infect. Control 34, S38-S45 (2006).
62. P. Ankomah, P. J. Johnson, B. R. Levin, The pharmaco, population and evolutionary dynamics of multi-drug therapy: Experiments with S. aureus and E. coli and computer simulations. PLOS Pathog. 9, e1003300 (2013).
63. R. R Core Team, R: A Language and Environment for Statistical Computing (available at http://www.R-project.org/).
64. J. C. Streibig, C. Ritz, Bioassay analysis using R. J. Stat. Softw. 12, 1-22 (2005) (available at http://econpapers.repec.org/RePEc:jss:jstsof:12:i05).
65. J. Lemon, Plotrix: A package in the red light district of R. R-News 6, 8-12 (2006).
66. H. Wickham, ggplot2: Elegant Graphics for Data Analysis (Springer Publishing Company Incorporated, New York, NY, 2009); http://dl.acm.org/citation.cfm?id=1795559.
67. B. Langmead, S. L. Salzberg, Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
68. A. R. Quinlan, I. M. Hall, BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
69. A. McKenna, M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, K. Garimella, D. Altshuler, S. Gabriel, M. Daly, M. A. DePristo, The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
70. M. A. DePristo, E. Banks, R. Poplin, K. V. Garimella, J. R. Maguire, C. Hartl, A. A. Philippakis, G. del Angel, M. A. Rivas, M. Hanna, A. McKenna, T. J. Fennell, A. M. Kernytsky, A. Y. Sivachenko, K. Cibulskis, S. B. Gabriel, D. Altshuler, M. J. Daly, A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
71. H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin; 1000 Genome Project Data Processing Subgroup, The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
72. H. Li, R. Durbin, Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
73. D. R. Zerbino, E. Birney, Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008).
74. P. J. Cock, T. Antao, J. T. Chang, B. A. Chapman, C. J. Cox, A. Dalke, I. Friedberg, T. Hamelryck, F. Kauff, B. Wilczynski, M. J. de Hoon, Biopython: Freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25, 1422-1423 (2009).
75. H. H. Wang, F. J. Isaacs, P. A. Carr, Z. Z. Sun, G. Xu, C. R. Forest, G. M. Church, Programming cells by multiplex genome engineering and accelerated evolution. Nature 460, 894-898 (2009).
76. H. H. Wang, G. M. Church, Multiplexed genome engineering and genotyping methods applications for synthetic biology and metabolic engineering. Methods Enzymol. 498, 409-426 (2011).