Activation of cryptic aminoglycoside resistance in Salmonella enterica

Molecular Microbiology

Volumn 80, Issue 6, 2011, Pages 1464-1478

  Koskiniemi, Sanna ^a   Pränting, Maria ^a   Gullberg, Erik ^a   Näsvall, Joakim ^a   Andersson, Dan I ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTIC AGENT; SPECTINOMYCIN; STREPTOMYCIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; DRUG MECHANISM; GENE ACTIVATION; GENE EXPRESSION; GENE LOCATION; GENE MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA ENTERICA; STOP CODON;

AMINOGLYCOSIDES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MUTATION; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; STREPTOMYCIN; TRANSCRIPTIONAL ACTIVATION; TRANSFERASES;

SALMONELLA ENTERICA; STRAWBERRY CRINKLE VIRUS;

EID: 79958839683     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07657.x     Document Type: Article

References (60)

1. Aravind, L., and Koonin, E.V. (1999) DNA polymerase beta-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res 27: 1609-1618.
2. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
3. Banky, J.P., Ostergaard, L., and Spelman, D. (2002) Chronic relapsing salmonella osteomyelitis in an immunocompetent patient: case report and literature review. J Infect 44: 44-47.
4. Baumert, N., von Eiff, C., Schaaff, F., Peters, G., Proctor, R.A., and Sahl, H.G. (2002) Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb Drug Resist 8: 253-260.
5. Beltran, P., Plock, S.A., Smith, N.H., Whittam, T.S., Old, D.C., and Selander, R.K. (1991) Reference collection of strains of the Salmonella typhimurium complex from natural populations. J Gen Microbiol 137: 601-606.
6. Block, R., and Haseltine, A.W. (1975) Purification and properties of stringent factor. J Biol Chem 250: 1212-1217.
7. Bryan, L.E., and Kwan, S. (1981) Aminoglycoside-resistant mutants of Pseudomonas aeruginosa deficient in cytochrome d, nitrite reductase, and aerobic transport. Antimicrob Agents Chemother 19: 958-964.
8. Cano, D.A., Pucciarelli, M.G., Martinez-Moya, M., Casadesus, J., and Garcia-del Portillo, F. (2003) Selection of small-colony variants of Salmonella enterica serovar typhimurium in nonphagocytic eucaryotic cells. Infect Immun 71: 3690-3698.
9. Carter, A.P., Clemons, W.M., Brodersen, D.E., Morgan-Warren, R.J., Wimberly, B.T., and Ramakrishnan, V. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407: 340-348.
10. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
11. Datta, S., Costantino, N., and Court, D.L. (2006) A set of recombineering plasmids for gram-negative bacteria. Gene 379: 109-115.
12. D'Costa, V.M., McGrann, K.M., Hughes, D.W., and Wright, G.D. (2006) Sampling the antibiotic resistome. Science 311: 374-377.
13. Gorini, L., and Kataja, E. (1964) Phenotypic repair by streptomycin of defective genotypes in E. coli. Proc Natl Acad Sci USA 51: 487-493.
14. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
15. Haugen, S.P., Ross, W., and Gourse, R.L. (2008) Advances in bacterial promoter recognition and its control by factors that do not bind DNA. Nat Rev Microbiol 6: 507-519.
16. Honoré, N., Marchal, G., and Cole, S.T. (1995) Novel mutation in 16S rRNA associated with streptomycin dependence in Mycobacterium tuberculosis. Antimicrob Agents Chemother 39: 769-770.
17. Kohler, C., von Eiff, C., Peters, G., Proctor, R.A., Hecker, M., and Engelmann, S. (2003) Physiological characterization of a heme-deficient mutant of Staphylococcus aureus by a proteomic approach. J Bacteriol 185: 6928-6937.
18. Koskiniemi, S., and Andersson, D.I. (2009) Translesion DNA polymerases are required for spontaneous deletion formation in Salmonella typhimurium. Proc Natl Acad Sci USA 106: 10248-10253.
19. Kotra, L.P., Haddad, J., and Mobashery, S. (2000) Aminoglycosides: perspectives on mechanisms of action and resistance and strategies to counter resistance. Antimicrob Agents Chemother 44: 3249-3256.
20. Laffler, T., and Gallant, J.A. (1974) Stringent control of protein synthesis in E. coli. Cell 3: 47-49.
21. Macinga, D.R., and Rather, P.N. (1996) aarD, a Providencia stuartii homologue of cydD: role in 2'-N-acetyltransferase expression, cell morphology and growth in the presence of an extracellular factor. Mol Microbiol 19: 511-520.
22. Macvanin, M., Johanson, U., Ehrenberg, M., and Hughes, D. (2000) Fusidic acid-resistant EF-G perturbs the accumulation of ppGpp. Mol Microbiol 37: 98-107.
23. Magnet, S., Courvalin, P., and Lambert, T. (1999) Activation of the cryptic aac(6')-Iy aminoglycoside resistance gene of Salmonella by a chromosomal deletion generating a transcriptional fusion. J Bacteriol 181: 6650-6655.
24. Maloy, S.R., Cronan, J.E., Jr, and Freifelder, D. (1994) Microbial Genetics. Boston, MA: Jones and Barlett Publishers International.
25. Miller, J.H. (1992) A Short Course in Bacterial Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Press.
26. Miller, J.H., Coulondre, C., and Farabaugh, P.J. (1978) Correlation of nonsense sites in the lacI gene with specific codons in the nucleotide sequence. Nature 274: 770-775.
27. Miller, M.H., Edberg, S.C., Mandel, L.J., Behar, C.F., and Steigbigel, N.H. (1980) Gentamicin uptake in wild-type and aminoglycoside-resistant small-colony mutants of Staphylococcus aureus. Antimicrob Agents Chemother 18: 722-729.
28. Milon, P., Tischenko, E., Tomsic, J., Caserta, E., Folkers, G., La Teana, A., etal. (2006) The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor. Proc Natl Acad Sci USA 103: 13962-13967.
29. Mitkevich, V.A., Ermakov, A., Kulikova, A.A., Tankov, S., Shyp, V., Soosaar, A., etal. (2010) Thermodynamic characterization of ppGpp binding to EF-G or IF2 and of initiator tRNA binding to free IF2 in the presence of GDP, GTP, or ppGpp. J Mol Biol 402: 838-846.
30. Morar, M., Bhullar, K., Hughes, D.W., Junop, M., and Wright, G.D. (2009) Structure and mechanism of the lincosamide antibiotic adenylyltransferase LinB. Structure 17: 1649-1659.
31. Murray, K.D., and Bremer, H. (1996) Control of spoT-dependent ppGpp synthesis and degradation in Escherichia coli. J Mol Biol 259: 41-57.
32. Newcombe, H.B., and Hawirko, R. (1949) Spontaneous mutation to streptomycin resistance and dependence in Escherichia coli. J Bacteriol 57: 565-572.
33. Nilsson, A.I., Zorzet, A., Kanth, A., Dahlstrom, S., Berg, O.G., and Andersson, D.I. (2006) Reducing the fitness cost of antibiotic resistance by amplification of initiator tRNA genes. Proc Natl Acad Sci USA 103: 6976-6981.
34. Okamoto, S., Tamaru, A., Nakajima, C., Nishimura, K., Tanaka, Y., Tokuyama, S., etal. (2007) Loss of a conserved 7-methylguanosine modification in 16S rRNA confers low-level streptomycin resistance in bacteria. Mol Microbiol 63: 1096-1106.
35. Ozaki, M., Mizushima, S., and Nomura, M. (1969) Identification and functional characterization of the protein controlled by the streptomycin-resistant locus in E. coli. Nature 222: 333-339.
36. Paul, B.J., Ross, W., Gaal, T., and Gourse, R.L. (2004) rRNA transcription in Escherichia coli. Annu Rev Genet 38: 749-770.
37. Paul, B.J., Berkmen, M.B., and Gourse, R.L. (2005) DksA potentiates direct activation of amino acid promoters by ppGpp. Proc Natl Acad Sci USA 102: 7823-7828.
38. Payie, K.G., and Clarke, A.J. (1997) Characterization of gentamicin 2'-N-acetyltransferase from Providencia stuartii: its use of peptidoglycan metabolites for acetylation of both aminoglycosides and peptidoglycan. J Bacteriol 179: 4106-4114.
39. Pedersen, L.C., Benning, M.M., and Holden, H.M. (1995) Structural investigation of the antibiotic and ATP-binding sites in kanamycin nucleotidyltransferase. Biochemistry 34: 13305-13311.
40. Potrykus, K., and Cashel, M. (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62: 35-51.
41. Pranting, M., and Andersson, D.I. (2010) Mechanisms and physiological effects of protamine resistance in Salmonella enterica serovar Typhimurium LT2. J Antimicrob Chemother 65: 876-887.
42. Proctor, R.A., van Langevelde, P., Kristjansson, M., Maslow, J.N., and Arbeit, R.D. (1995) Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 20: 95-102.
43. Proctor, R.A., von Eiff, C., Kahl, B.C., Becker, K., McNamara, P., Herrmann, M., and Peters, G. (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4: 295-305.
44. Rather, P.N. (1998) Origins of the aminoglycoside modifying enzymes. Drug Resist Updat 1: 285-291.
45. Rather, P.N., Orosz, E., Shaw, K.J., Hare, R., and Miller, G. (1993) Characterization and transcriptional regulation of the 2'-N-acetyltransferase gene from Providencia stuartii. J Bacteriol 175: 6492-6498.
46. Rather, P.N., Solinsky, K.A., Paradise, M.R., and Parojcic, M.M. (1997) aarC, an essential gene involved in density-dependent regulation of the 2'-N-acetyltransferase in Providencia stuartii. J Bacteriol 179: 2267-2273.
47. Ruusala, T., and Kurland, C.G. (1984) Streptomycin preferentially perturbs ribosomal proofreading. Mol Gen Genet 198: 100-104.
48. Ruusala, T., Andersson, D., Ehrenberg, M., and Kurland, C.G. (1984) Hyper-accurate ribosomes inhibit growth. EMBO J 3: 2575-2580.
49. Sadowska, B., Bonar, A., von Eiff, C., Proctor, R.A., Chmiela, M., Rudnicka, W., and Rozalska, B. (2002) Characteristics of Staphylococcus aureus, isolated from airways of cystic fibrosis patients, and their small colony variants. FEMS Immunol Med Microbiol 32: 191-197.
50. Schreiber, G., Metzger, S., Aizenman, E., Roza, S., Cashel, M., and Glaser, G. (1991) Overexpression of the relA gene in Escherichia coli. J Biol Chem 266: 3760-3767.
51. Simons, R.W., Houman, F., and Kleckner, N. (1987) Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53: 85-96.
52. Soo, V.W., Hanson-Manful, P., and Patrick, W.M. (2010) Artificial gene amplification reveals an abundance of promiscuous resistance determinants in Escherichia coli. Proc Natl Acad Sci USA 108: 1484-1489.
53. Springer, B., Kidan, Y.G., Prammananan, T., Ellrott, K., Bottger, E.C., and Sander, P. (2001) Mechanisms of streptomycin resistance: selection of mutations in the 16S rRNA gene conferring resistance. Antimicrob Agents Chemother 45: 2877-2884.
54. Stephens, J.C., Artz, S.W., and Ames, B.N. (1975) Guanosine 5'-diphosphate 3'-diphosphate (ppGpp): positive effector for histidine operon transcription and general signal for amino-acid deficiency. Proc Natl Acad Sci USA 72: 4389-4393.
55. Udou, T., Mizuguchi, Y., and Wallace, R.J., Jr (1989) Does aminoglycoside-acetyltransferase in rapidly growing mycobacteria have a metabolic function in addition to aminoglycoside inactivation? FEMS Microbiol Lett 48: 227-230.
56. Vakulenko, S.B., and Mobashery, S. (2003) Versatility of aminoglycosides and prospects for their future. Clin Microbiol Rev 16: 430-450.
57. Whitman, W.B., Coleman, D.C., and Wiebe, W.J. (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95: 6578-6583.
58. Winston, F., Botstein, D., and Miller, J.H. (1979) Characterization of amber and ochre suppressors in Salmonella typhimurium. J Bacteriol 137: 433-439.
59. Wright, G.D. (2010) The antibiotic resistome. Expert Opin Drug Discov 5: 779-788.
60. Xiao, H., Kalman, M., Ikehara, K., Zemel, S., Glaser, G., and Cashel, M. (1991) Residual guanosine 3', 5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J Biol Chem 266: 5980-5990.