Molecular mechanisms and clinical impact of acquired and intrinsic fosfomycin resistance

Antibiotics

Volumn 2, Issue 2, 2013, Pages 217-236

  Castañeda García, Alfredo ^a   Blázquez, Jesús ^b   Rodríguez Rojas, Alexandro ^c  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Fosfomycin resistance; Molecular mechanisms

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; CARRIER PROTEIN; CYCLIC AMP; FOSFOMYCIN; FOSX HYDROLASE; GLYCEROL 3 PHOSPHATE TRANSPORTER; GLYCEROL 6 PHOSPHATE TRANSPORTER; HYDROLASE; PROTEIN FOSA; PROTEIN FOSX; PROTEIN MURA; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; BACTERIAL INFECTION; CELL MEMBRANE PERMEABILITY; CHEMICAL MODIFICATION; DRUG MECHANISM; DRUG PENETRATION; GENE MUTATION; HUMAN; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; URINARY TRACT INFECTION;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 84902209071     PISSN: None     EISSN: 20796382     Source Type: Journal    
DOI: 10.3390/antibiotics2020217     Document Type: Review

References (106)

1. Nathan, C. Antibiotics at the crossroads. Nature 2004, 431, 899-902.
2. Livermore, D. M. Has the era of untreatable infections arrived? J. Antimicrob. Chemother. 2009, 64 (Suppl. 1), 29-36.
3. Falagas, M. E.; Grammatikos, A. P.; Michalopoulos, A. Potential of old-generation antibiotics to address current need for new antibiotics. Expert Rev. Anti. Infect. Ther. 2008, 6, 593-600.
4. Hendlin, D.; Stapley, E. O.; Jackson, M.; Wallick, H.; Miller, A. K.; Wolf, F. J.; Miller, T. W.; Chaiet, L.; Kahan, F. M.; Foltz, E. L.; et al. Phosphonomycin, a new antibiotic produced by strains of Streptomyces. Science 1969, 166, 122-123.
5. Kahan, F. M.; Kahan, J. S.; Cassidy, P. J.; Kropp, H. The mechanism of action of fosfomycin (phosphonomycin). Ann. NY Acad. Sci. 1974, 235, 364-386.
6. Wagenlehner, F. M.; Hoyme, U.; Kaase, M.; Funfstuck, R.; Naber, K. G.; Schmiemann, G. Uncomplicated urinary tract infections. Dtsch. Arztebl. Int. 2011, 108, 415-423.
7. Schito, G. C. Why fosfomycin trometamol as first line therapy for uncomplicated UTI? Int. J. Antimicrob. Agents 2003, 22 (Suppl. 2), 79-83.
8. Falagas, M. E.; Giannopoulou, K. P.; Kokolakis, G. N.; Rafailidis, P. I. Fosfomycin: Use beyond urinary tract and gastrointestinal infections. Clin. Infect. Dis. 2008, 46, 1069-1077.
9. Barry, A. L.; Brown, S. D. Antibacterial spectrum of fosfomycin trometamol. J. Antimicrob. Chemother. 1995, 35, 228-230.
10. Lu, C. L.; Liu, C. Y.; Huang, Y. T.; Liao, C. H.; Teng, L. J.; Turnidge, J. D.; Hsueh, P. R. Antimicrobial susceptibilities of commonly encountered bacterial isolates to fosfomycin determined by agar dilution and disk diffusion methods. Antimicrob. Agents Chemother. 2011, 55, 4295-4301.
11. Falagas, M. E.; Kastoris, A. C.; Karageorgopoulos, D. E.; Rafailidis, P. I. Fosfomycin for the treatment of infections caused by multidrug-resistant non-fermenting gram-negative bacilli: A systematic review of microbiological, animal and clinical studies. Int. J. Antimicrob. Agents 2009, 34, 111-120.
12. Neuner, E. A.; Sekeres, J.; Hall, G. S.; van Duin, D. Experience with fosfomycin for treatment of urinary tract infections due to multidrug-resistant organisms. Antimicrob. Agents Chemother. 2012, 56, 5744-5748.
13. Falagas, M. E.; Kastoris, A. C.; Kapaskelis, A. M.; Karageorgopoulos, D. E. Fosfomycin for the treatment of multidrug-resistant, including extended-spectrum beta-lactamase producing, Enterobacteriaceae infections: A systematic review. Lancet Infect. Dis. 2010, 10, 43-50.
14. Brown, E. D.; Vivas, E. I.; Walsh, C. T.; Kolter, R. MurA (MurZ), the enzyme that catalyzes the first committed step in peptidoglycan biosynthesis, is essential in Escherichia coli. J. Bacteriol. 1995, 177, 4194-4197.
15. Marquardt, J. L.; Brown, E. D.; Lane, W. S.; Haley, T. M.; Ichikawa, Y.; Wong, C. H.; Walsh, C. T. Kinetics, stoichiometry, and identification of the reactive thiolate in the inactivation of UDP-GlcNAc enolpyruvoyl transferase by the antibiotic fosfomycin. Biochemistry 1994, 33, 10646-10651.
16. Skarzynski, T.; Mistry, A.; Wonacott, A.; Hutchinson, S. E.; Kelly, V. A.; Duncan, K. Structure of UDP-N-acetylglucosamine enolpyruvyl transferase, an enzyme essential for the synthesis of bacterial peptidoglycan, complexed with substrate UDP-N-acetylglucosamine and the drug fosfomycin. Structure 1996, 4, 1465-1474.
17. Kadner, R. J.; Winkler, H. H. Isolation and characterization of mutations affecting the transport of hexose phosphates in Escherichia coli. J. Bacteriol. 1973, 113, 895-900.
18. Tsuruoka, T.; Yamada, Y. Charactertization of spontaneous fosfomycin (phosphonomycin)-resistant cells of Escherichia coli B in vitro. J. Antibiot. (Tokyo) 1975, 28, 906-911.
19. Grimm, H. In vitro investigations with fosfomycin on Mueller-Hinton agar with and without glucose-6-phosphate. Infection 1979, 7, 256-259.
20. Castaneda-Garcia, A.; Rodriguez-Rojas, A.; Guelfo, J. R.; Blazquez, J. The glycerol-3-phosphate permease GlpT is the only fosfomycin transporter in Pseudomonas aeruginosa. J. Bacteriol. 2009, 191, 6968-6974.
21. Schweizer, H. P.; Po, C. Regulation of glycerol metabolism in Pseudomonas aeruginosa: Characterization of the glpR repressor gene. J. Bacteriol. 1996, 178, 5215-5221.
22. Scortti, M.; Lacharme-Lora, L.; Wagner, M.; Chico-Calero, I.; Losito, P.; Vazquez-Boland, J. A. Coexpression of virulence and fosfomycin susceptibility in Listeria: Molecular basis of an antimicrobial in vitro-in vivo paradox. Nat. Med. 2006, 12, 515-517.
23. Chico-Calero, I.; Suarez, M.; Gonzalez-Zorn, B.; Scortti, M.; Slaghuis, J.; Goebel, W.; Vazquez-Boland, J. A. Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc. Natl. Acad. Sci. USA 2002, 99, 431-436.
24. Lemieux, M. J.; Huang, Y.; Wang, D. N. Glycerol-3-phosphate transporter of Escherichia coli: Structure, function and regulation. Res. Microbiol. 2004, 155, 623-629.
25. Huang, Y.; Lemieux, M. J.; Song, J.; Auer, M.; Wang, D. N. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 2003, 301, 616-620.
26. Lemieux, M. J.; Huang, Y.; Wang, D. N. The structural basis of substrate translocation by the Escherichia coli glycerol-3-phosphate transporter: A member of the major facilitator superfamily. Curr. Opin. Struct. Biol. 2004, 14, 405-412.
27. Elvin, C. M.; Hardy, C. M.; Rosenberg, H. Pi exchange mediated by the glpt-dependent sn-glycerol-3-phosphate transport system in Escherichia coli. J. Bacteriol. 1985, 161, 1054-1058.
28. Hardisson, C.; Llaneza, J. The action of fosfomycin on the growth of Pseudomonas aeruginosa. Chemotherapy 1977, 23 (Suppl. 1), 37-44.
29. Lindgren, V. Mapping of a genetic locus that affects glycerol 3-phosphate transport in Bacillus subtilis. J. Bacteriol. 1978, 133, 667-670.
30. Santoro, A.; Cappello, A. R.; Madeo, M.; Martello, E.; Iacopetta, D.; Dolce, V. Interaction of fosfomycin with the glycerol 3-phosphate transporter of Escherichia coli. Biochim. Biophys. Acta 2011, 1810, 1323-1329.
31. Larson, T. J.; Ye, S. Z.; Weissenborn, D. L.; Hoffmann, H. J.; Schweizer, H. Purification and characterization of the repressor for the sn-glycerol 3-phosphate regulon of Escherichia coli K-12. J. Biol. Chem. 1987, 262, 15869-15874.
32. Yang, B.; Gerhardt, S. G.; Larson, T. J. Action at a distance for glp repressor control of glpTQ transcription in Escherichia coli K-12. Mol. Microbiol. 1997, 24, 511-521.
33. Zeng, G.; Ye, S.; Larson, T. J. Repressor for the sn-glycerol 3-phosphate regulon of Escherichia coli K-12: Primary structure and identification of the DNA-binding domain. J. Bacteriol. 1996, 178, 7080-7089.
34. Kadner, R. J.; Shattuck-Eidens, D. M. Genetic control of the hexose phosphate transport system of Escherichia coli: Mapping of deletion and insertion mutations in the uhp region. J. Bacteriol. 1983, 155, 1052-1061.
35. Sonna, L. A.; Ambudkar, S. V.; Maloney, P. C. The mechanism of glucose 6-phosphate transport by Escherichia coli. J. Biol. Chem. 1988, 263, 6625-6630.
36. Eiglmeier, K.; Boos, W.; Cole, S. T. Nucleotide sequence and transcriptional startpoint of the glpT gene of Escherichia coli: Extensive sequence homology of the glycerol-3-phosphate transport protein with components of the hexose-6-phosphate transport system. Mol. Microbiol. 1987, 1, 251-258.
37. Ambudkar, S. V.; Anantharam, V.; Maloney, P. C. UhpT, the sugar phosphate antiporter of Escherichia coli, functions as a monomer. J. Biol. Chem. 1990, 265, 12287-12292.
38. Lloyd, A. D.; Kadner, R. J. Topology of the Escherichia coli uhpT sugar-phosphate transporter analyzed by using TnphoA fusions. J. Bacteriol. 1990, 172, 1688-1693.
39. Island, M. D.; Kadner, R. J. Interplay between the membrane-associated UhpB and UhpC regulatory proteins. J. Bacteriol. 1993, 175, 5028-5034.
40. Chen, Q.; Kadner, R. J. Effect of altered spacing between uhpT promoter elements on transcription activation. J. Bacteriol. 2000, 182, 4430-4436.
41. Dahl, J. L.; Wei, B. Y.; Kadner, R. J. Protein phosphorylation affects binding of the Escherichia coli transcription activator UhpA to the uhpT promoter. J. Biol. Chem. 1997, 272, 1910-1919.
42. Olekhnovich, I. N.; Kadner, R. J. Mutational scanning and affinity cleavage analysis of UhpA-binding sites in the Escherichia coli uhpT promoter. J. Bacteriol. 2002, 184, 2682-2691.
43. Alper, M. D.; Ames, B. N. Transport of antibiotics and metabolite analogs by systems under cyclic AMP control: Positive selection of Salmonella typhimurium cya and crp mutants. J. Bacteriol. 1978, 133, 149-157.
44. Cordaro, J. C.; Melton, T.; Stratis, J. P.; Atagun, M.; Gladding, C.; Hartman, P. E.; Roseman, S. Fosfomycin resistance: Selection method for internal and extended deletions of the phosphoenolpyruvate: Sugar phosphotransferase genes of Salmonella typhimurium. J. Bacteriol. 1976, 128, 785-793.
45. Sakamoto, Y.; Furukawa, S.; Ogihara, H.; Yamasaki, M. Fosmidomycin resistance in adenylate cyclase deficient (cya) mutants of Escherichia coli. Biosci. Biotechnol. Biochem. 2003, 67, 2030-2033.
46. Tsuruoka, T.; Miyata, A.; Yamada, Y. Two kinds of mutants defective in multiple carbohydrate utilization isolated from in vitro fosfomycin-resistant strains of Escherichia coli K-12. J. Antibiot. (Tokyo) 1978, 31, 192-201.
47. Larson, T. J.; Cantwell, J. S.; van Loo-Bhattacharya, A. T. Interaction at a distance between multiple operators controls the adjacent, divergently transcribed glpTQ-glpACB operons of Escherichia coli K-12. J. Biol. Chem. 1992, 267, 6114-6121.
48. Merkel, T. J.; Dahl, J. L.; Ebright, R. H.; Kadner, R. J. Transcription activation at the Escherichia coli uhpT promoter by the catabolite gene activator protein. J. Bacteriol. 1995, 177, 1712-1718.
49. Olekhnovich, I. N.; Dahl, J. L.; Kadner, R. J. Separate contributions of UhpA and CAP to activation of transcription of the uhpT promoter of Escherichia coli. J. Mol. Biol. 1999, 292, 973-986.
50. Kim, D. H.; Lees, W. J.; Kempsell, K. E.; Lane, W. S.; Duncan, K.; Walsh, C. T. Characterization of a Cys115 to Asp substitution in the Escherichia coli cell wall biosynthetic enzyme UDP-GlcNAc enolpyruvyl transferase (MurA) that confers resistance to inactivation by the antibiotic fosfomycin. Biochemistry 1996, 35, 4923-4928.
51. Brown, E. D.; Marquardt, J. L.; Lee, J. P.; Walsh, C. T.; Anderson, K. S. Detection and characterization of a phospholactoyl-enzyme adduct in the reaction catalyzed by UDP-N-acetylglucosamine enolpyruvoyl transferase, MurZ. Biochemistry 1994, 33, 10638-10645.
52. Ramilo, C.; Appleyard, R. J.; Wanke, C.; Krekel, F.; Amrhein, N.; Evans, J. N. Detection of the covalent intermediate of UDP-N-acetylglucosamine enolpyruvyl transferase by solution-state and time-resolved solid-state NMR spectroscopy. Biochemistry 1994, 33, 15071-15079.
53. Wanke, C.; Amrhein, N. Evidence that the reaction of the UDP-N-acetylglucosamine 1-carboxyvinyltransferase proceeds through the O-phosphothioketal of pyruvic acid bound to Cys115 of the enzyme. Eur. J. Biochem. 1993, 218, 861-870.
54. Eschenburg, S.; Priestman, M.; Schonbrunn, E. Evidence that the fosfomycin target Cys115 in UDP-N-acetylglucosamine enolpyruvyl transferase (MurA) is essential for product release. J. Biol. Chem. 2005, 280, 3757-3763.
55. De Smet, K. A.; Kempsell, K. E.; Gallagher, A.; Duncan, K.; Young, D. B. Alteration of a single amino acid residue reverses fosfomycin resistance of recombinant MurA from Mycobacterium tuberculosis. Microbiology 1999, 145, 3177-3184.
56. Jiang, S.; Gilpin, M. E.; Attia, M.; Ting, Y. L.; Berti, P. J. Lyme disease enolpyruvyl-udp-glcnac synthase: Fosfomycin-resistant MurA from Borrelia burgdorferi, a fosfomycin-sensitive mutant, and the catalytic role of the active site Asp. Biochemistry 2011, 50, 2205-2212.
57. McCoy, A. J.; Sandlin, R. C.; Maurelli, A. T. In vitro and in vivo functional activity of Chlamydia MurA, a UDP-N-acetylglucosamine enolpyruvyl transferase involved in peptidoglycan synthesis and fosfomycin resistance. J. Bacteriol. 2003, 185, 1218-1228.
58. Venkateswaran, P. S.; Wu, H. C. Isolation and characterization of a phosphonomycin-resistant mutant of Escherichia coli K-12. J. Bacteriol. 1972, 110, 935-944.
59. Takahata, S.; Ida, T.; Hiraishi, T.; Sakakibara, S.; Maebashi, K.; Terada, S.; Muratani, T.; Matsumoto, T.; Nakahama, C.; Tomono, K. Molecular mechanisms of fosfomycin resistance in clinical isolates of Escherichia coli. Int. J. Antimicrob. Agents 2010, 35, 333-337.
60. Marquardt, J. L.; Siegele, D. A.; Kolter, R.; Walsh, C. T. Cloning and sequencing of Escherichia coli MurZ and purification of its product, a UDP-N-acetylglucosamine enolpyruvyl transferase. J. Bacteriol. 1992, 174, 5748-5752.
61. Couce, A.; Briales, A.; Rodriguez-Rojas, A.; Costas, C.; Pascual, A.; Blazquez, J. Genomewide overexpression screen for fosfomycin resistance in Escherichia coli: MurA confers clinical resistance at low fitness cost. Antimicrob. Agents Chemother. 2012, 56, 2767-2769.
62. Horii, T.; Kimura, T.; Sato, K.; Shibayama, K.; Ohta, M. Emergence of fosfomycin-resistant isolates of shiga-like toxin-producing Escherichia coli O26. Antimicrob. Agents Chemother. 1999, 43, 789-793.
63. Rigsby, R. E.; Fillgrove, K. L.; Beihoffer, L. A.; Armstrong, R. N. Fosfomycin resistance proteins: A nexus of glutathione transferases and epoxide hydrolases in a metalloenzyme superfamily. Meth. Enzymol. 2005, 401, 367-379.
64. Brown, D. W.; Schaab, M. R.; Birmingham, W. R.; Armstrong, R. N. Evolution of the antibiotic resistance protein, FosA, is linked to a catalytically promiscuous progenitor. Biochemistry 2009, 48, 1847-1849.
65. Armstrong, R. N. Mechanistic imperatives for the evolution of glutathione transferases. Curr. Opin. Chem. Biol. 1998, 2, 618-623.
66. Armstrong, R. N. Mechanistic diversity in a metalloenzyme superfamily. Biochemistry 2000, 39, 13625-13632.
67. Leon, J.; Garcia-Lobo, J. M.; Navas, J.; Ortiz, J. M. Fosfomycin-resistance plasmids determine an intracellular modification of fosfomycin. J. Gen. Microbiol. 1985, 131, 1649-1655.
68. Llaneza, J.; Villar, C. J.; Salas, J. A.; Suarez, J. E.; Mendoza, M. C.; Hardisson, C. Plasmid-mediated fosfomycin resistance is due to enzymatic modification of the antibiotic. Antimicrob. Agents Chemother. 1985, 28, 163-164.
69. Mendoza, C.; Garcia, J. M.; Llaneza, J.; Mendez, F. J.; Hardisson, C.; Ortiz, J. M. Plasmid-determined resistance to fosfomycin in Serratia marcescens. Antimicrob. Agents Chemother. 1980, 18, 215-219.
70. Garcia-Lobo, J. M.; Ortiz, J. M. Tn292l, a transposon encoding fosfomycin resistance. J. Bacteriol. 1982, 151, 477-479.
71. Seoane, A.; Sangari, F. J.; Lobo, J. M. Complete nucleotide sequence of the fosfomycin resistance transposon Tn2921. Int. J. Antimicrob. Agents 2010, 35, 413-414.
72. Rife, C. L.; Pharris, R. E.; Newcomer, M. E.; Armstrong, R. N. Crystal structure of a genomically encoded fosfomycin resistance protein (FosA) at 1. 19 A resolution by MAD phasing off the L-III edge of Tl(+). J. Am. Chem. Soc. 2002, 124, 11001-11003.
73. Arca, P.; Hardisson, C.; Suarez, J. E. Purification of a glutathione S-transferase that mediates fosfomycin resistance in bacteria. Antimicrob. Agents Chemother. 1990, 34, 844-848.
74. Arca, P.; Rico, M.; Brana, A. F.; Villar, C. J.; Hardisson, C.; Suarez, J. E. Formation of an adduct between fosfomycin and glutathione: A new mechanism of antibiotic resistance in bacteria. Antimicrob. Agents Chemother. 1988, 32, 1552-1556.
75. Bernat, B. A.; Laughlin, L. T.; Armstrong, R. N. Fosfomycin resistance protein (FosA) is a manganese metalloglutathione transferase related to glyoxalase I and the extradiol dioxygenases. Biochemistry 1997, 36, 3050-3055.
76. Bernat, B. A.; Armstrong, R. N. Elementary steps in the acquisition of Mn2+ by the fosfomycin resistance protein (FosA). Biochemistry 2001, 40, 12712-12718.
77. Bernat, B. A.; Laughlin, L. T.; Armstrong, R. N. Elucidation of a monovalent cation dependence and characterization of the divalent cation binding site of the fosfomycin resistance protein (FosA). Biochemistry 1999, 38, 7462-7469.
78. Beharry, Z.; Palzkill, T. Functional analysis of active site residues of the fosfomycin resistance enzyme FosA from Pseudomonas aeruginosa. J. Biol. Chem. 2005, 280, 17786-17791.
79. Etienne, J.; Gerbaud, G.; Fleurette, J.; Courvalin, P. Characterization of staphylococcal plasmids hybridizing with the fosfomycin resistance gene fosB. FEMS Microbiol. Lett. 1991, 68, 119-122.
80. Zilhao, R.; Courvalin, P. Nucleotide sequence of the fosB gene conferring fosfomycin resistance in Staphylococcus epidermidis. FEMS Microbiol. Lett. 1990, 56, 267-272.
81. Cao, M.; Bernat, B. A.; Wang, Z.; Armstrong, R. N.; Helmann, J. D. FosB, a cysteine-dependent fosfomycin resistance protein under the control of sigma(W), an extracytoplasmic-function sigma factor in Bacillus subtilis. J. Bacteriol. 2001, 183, 2380-2383.
82. Butcher, B. G.; Helmann, J. D. Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol. Microbiol. 2006, 60, 765-782.
83. Gaballa, A.; Newton, G. L.; Antelmann, H.; Parsonage, D.; Upton, H.; Rawat, M.; Claiborne, A.; Fahey, R. C.; Helmann, J. D. Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in Bacilli. Proc. Natl. Acad. Sci. USA 2010, 107, 6482-6486.
84. Parsonage, D.; Newton, G. L.; Holder, R. C.; Wallace, B. D.; Paige, C.; Hamilton, C. J.; Dos Santos, P. C.; Redinbo, M. R.; Reid, S. D.; Claiborne, A. Characterization of the N-acetyl-alpha-D-glucosaminyl l-malate synthase and deacetylase functions for bacillithiol biosynthesis in Bacillus anthracis. Biochemistry 2010, 49, 8398-8414.
85. Roberts, A. A.; Sharma, S. V.; Strankman, A. W.; Duran, S. R.; Rawat, M.; Hamilton, C. J. Mechanistic studies of FosB: A divalent metal-dependent bacillithiol-S-transferase that mediates fosfomycin resistance in Staphylococcus aureus. Biochem. J. 2013, 451, 69-79.
86. Fillgrove, K. L.; Pakhomova, S.; Newcomer, M. E.; Armstrong, R. N. Mechanistic diversity of fosfomycin resistance in pathogenic microorganisms. J. Am. Chem. Soc. 2003, 125, 15730-15731.
87. Fillgrove, K. L.; Pakhomova, S.; Schaab, M. R.; Newcomer, M. E.; Armstrong, R. N. Structure and mechanism of the genomically encoded fosfomycin resistance protein, FosX, from Listeria monocytogenes. Biochemistry 2007, 46, 8110-8120.
88. Kobayashi, S.; Kuzuyama, T.; Seto, H. Characterization of the fomA and fomB gene products from Streptomyces wedmorensis, which confer fosfomycin resistance on Escherichia coli. Antimicrob. Agents Chemother. 2000, 44, 647-650.
89. Kuzuyama, T.; Kobayashi, S.; O'Hara, K.; Hidaka, T.; Seto, H. Fosfomycin monophosphate and fosfomycin diphosphate, two inactivated fosfomycin derivates formed by gene products of fomA and fomB from a fosfomycin producing organism Streptomyces wedmorensis. J. Antibiot. (Tokyo) 1996, 49, 502-504.
90. Pakhomova, S.; Bartlett, S. G.; Augustus, A.; Kuzuyama, T.; Newcomer, M. E. Crystal structure of fosfomycin resistance kinase FomA from Streptomyces wedmorensis. J. Biol. Chem. 2008, 283, 28518-28526.
91. Garcia, P.; Arca, P.; Evaristo Suarez, J. Product of fosC, a gene from Pseudomonas syringae, mediates fosfomycin resistance by using ATP as cosubstrate. Antimicrob. Agents Chemother. 1995, 39, 1569-1573.
92. Kim, S. Y.; Ju, K. S.; Metcalf, W. W.; Evans, B. S.; Kuzuyama, T.; van der Donk, W. A. Different biosynthetic pathways to fosfomycin in Pseudomonas syringae and Streptomyces species. Antimicrob. Agents Chemother. 2012, 56, 4175-4183.
93. Arca, P.; Reguera, G.; Hardisson, C. Plasmid-encoded fosfomycin resistance in bacteria isolated from the urinary tract in a multicentre survey. J. Antimicrob. Chemother. 1997, 40, 393-399.
94. O'Hara, K. Two different types of fosfomycin resistance in clinical isolates of Klebsiella pneumoniae. FEMS Microbiol. Lett. 1993, 114, 9-16.
95. Shimizu, M.; Shigeobu, F.; Miyakozawa, I.; Nakamura, A.; Suzuki, M.; Mizukoshi, S.; O'Hara, K.; Sawai, T. Novel fosfomycin resistance of Pseudomonas aeruginosa clinical isolates recovered in Japan in 1996. Antimicrob. Agents Chemother. 2000, 44, 2007-2008.
96. Wachino, J.; Yamane, K.; Suzuki, S.; Kimura, K.; Arakawa, Y. Prevalence of fosfomycin resistance among CTX-M-producing Escherichia coli clinical isolates in Japan and identification of novel plasmid-mediated fosfomycin-modifying enzymes. Antimicrob. Agents Chemother. 2010, 54, 3061-3064.
97. Ho, P. L.; Chan, J.; Lo, W. U.; Law, P. Y.; Chow, K. H. Plasmid-mediated fosfomycin resistance in Escherichia coli isolated from pig. Vet. Microbiol. 2013, 162, 964-967.
98. Ho, P. L.; Chan, J.; Lo, W. U.; Law, P. Y.; Li, Z.; Lai, E. L.; Chow, K. H., Dissemination of plasmid-mediated fosfomycin resistance fosA3 among multidrug-resistant Escherichia coli from livestock and other animals. J. Appl. Microbiol. 2013, 114, 695-702.
99. Hou, J.; Huang, X.; Deng, Y.; He, L.; Yang, T.; Zeng, Z.; Chen, Z.; Liu, J. H. Dissemination of the fosfomycin resistance gene fosA3 with CTX-M beta-lactamase genes and rmtB carried on IncFII plasmids among Escherichia coli isolates from pets in China. Antimicrob. Agents Chemother. 2012, 56, 2135-2138.
100. He, L.; Partridge, S. R.; Yang, X.; Hou, J.; Deng, Y.; Yao, Q.; Zeng, Z.; Chen, Z.; Liu, J. H. Complete nucleotide sequence of pHN7A8, an F33: A-: B-type epidemic plasmid carrying blaCTX-M-65, fosA3 and rmtB from China. J. Antimicrob. Chemother. 2013, 68, 46-50.
101. Shen, P.; Jiang, Y.; Zhou, Z.; Zhang, J.; Yu, Y.; Li, L. Complete nucleotide sequence of pKP96, a 67 850 bp multiresistance plasmid encoding qnrA1, aac(6')-Ib-cr and blaCTX-M-24 from Klebsiella pneumonia. J. Antimicrob. Chemother. 2008, 62, 1252-1256.
102. Lee, S. Y.; Park, Y. J.; Yu, J. K.; Jung, S.; Kim, Y.; Jeong, S. H.; Arakawa, Y. Prevalence of acquired fosfomycin resistance among extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae clinical isolates in Korea and IS26-composite transposon surrounding fosA3. J. Antimicrob. Chemother. 2012, 60, 329-336.
103. De Groote, V. N.; Fauvart, M.; Kint, C. I.; Verstraeten, N.; Jans, A.; Cornelis, P.; Michiels, J. Pseudomonas aeruginosa fosfomycin resistance mechanisms affect non-inherited fluoroquinolone tolerance. J. Med. Microbiol. 2011, 60, 329-336.
104. Nilsson, A. I.; Berg, O. G.; Aspevall, O.; Kahlmeter, G.; Andersson, D. I. Biological costs and mechanisms of fosfomycin resistance in Escherichia coli. Antimicrob. Agents Chemother. 2003, 47, 2850-2858.
105. Oteo, J.; Orden, B.; Bautista, V.; Cuevas, O.; Arroyo, M.; Martinez-Ruiz, R.; Perez-Vazquez, M.; Alcaraz, M.; Garcia-Cobos, S.; Campos, J. CTX-M-15-producing urinary Escherichia coli O25b-ST131-phylogroup B2 has acquired resistance to fosfomycin. J. Antimicrob. Chemother. 2009, 64, 712-717.
106. Rodriguez-Rojas, A.; Macia, M. D.; Couce, A.; Gomez, C.; Castaneda-Garcia, A.; Oliver, A.; Blazquez, J. Assesing the emergence of resistance: The absence of biological cost in vivo may compromise fosfomycin treatments for Pseudomonas aeruginosa infections. PLoS One 2010, 5, e10193.