From “an enzyme able to destroy penicillin” to Carbapenemases: 70 Years of Beta-lactamase Misbehaviour

Current Drug Targets

Volumn 17, Issue 9, 2016, Pages 974-982

  Frère, Jean Marie ^a   Sauvage, Eric ^a   Kerff, Frédéric ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Carbapenemase(s); Cephalosporins; Penicillins; lactamase(s)

Indexed keywords

AMPICILLIN; BETA LACTAMASE; BIAPENEM; BINDING PROTEIN; CARBAPENEM; CARBAPENEMASE; CEFEPIME; CEFOTAXIME; CEFOXITIN; CEFTAZIDIME; IMIPENEM; MEROPENEM; METALLO BETA LACTAMASE; METICILLIN; PENICILLIN DERIVATIVE; PENICILLIN G; PENICILLIN V; PENICILLINASE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CARBAPENEM DERIVATIVE;

AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL MODIFICATION; CHEMICAL STRUCTURE; ENTEROBACTERIACEAE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HUMAN; HYDROLYSIS; NONHUMAN; PROTEIN EXPRESSION; R FACTOR; STAPHYLOCOCCUS AUREUS; BACTERIUM; CHEMISTRY; DRUG DEVELOPMENT; DRUG EFFECTS; ENZYMOLOGY; HISTORY; METABOLISM; MOLECULAR MODEL;

ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL PROTEINS; BETA-LACTAMASES; CARBAPENEMS; DRUG DISCOVERY; DRUG RESISTANCE, BACTERIAL; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; MODELS, MOLECULAR;

EID: 84973598714     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/1389450116666151001112859     Document Type: Article

References (99)

1. Fleming A. On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenza. British J Exp Pathol 1929; 10: 226-36.
2. Abraham EP. Sir Robert Robinson and the early history of penicillin. Nat Prod Rep 1987; 4: 41-6.
3. Crowfoot D, Bunn CW, Rogers-Low BW, Turner-Jones. x-rays crystanographic investigation of the structure of the penicillin. In: A, Clarke HT, Johnson JR, Robinson R, Eds: The chemistry of penicillin Princeton: Princeton University Press 1949; pp. 310-67.
4. Hodgkin DC. The X-ray analysis of the structure of penicillin. Adv Sci 1949; 6: 85-9.
5. Abraham EP, Chain E. An enzyme from bacteria able to destroy penicillin. Nature 1940; 146: 837.
6. Pollock MR. The function and evolution of penicillinase. Proc R Soc London B 1971; 179: 385-401.
7. Aronson JK. Penicillin. Eur J Clin Pharmacol 1992; 42: 1-9.
8. Barber M, Waterworth PM. Antibacterial activity of the penicillins. Brit Med J 1962; 1: 1159-64.
9. Barber M. Methicillin-resistant staphylococci. J Clin Pathol 1961; 14: 385-93.
10. Datta N, Kontomichalou P. Penicillinase synthesis controlled by infectious R factors in Enterobacteriaceae. Nature 1965; 208: 239- 41.
11. Datta N, Richmond MH. The purification and properties of a penicillinase whose synthesis is mediated by an R-factor in Escherichia coli. Biochem J 1966; 98: 204-9.
12. Philippon A, Labia R, Jacoby G. Extended-spectrum betalactamases. Antimicro Agents Chemother 1989; 33: 1131-6.
13. Raquet X, Lamotte-Brasseur J, Fonzé E, Goussard S, Courvalin P, Frère JM. TEM beta-lactamase mutants hydrolysing thirdgeneration cephalosporins. A kinetic and molecular modelling analysis. J Mol Biol 1994; 244: 625-39.
14. Reading C, Cole M. Clavulanic acid: a beta-lactamase-inhibiting beta-lactam from Streptomyces clavuligerus. Antimicro Agents Chemother 1977; 11: 852-7.
15. English AR, Retsema JA, Girard AE, Lynch JE, Barth WE. CP- 45,899, a beta-lactamase inhibitor that extends the antibacterial spectrum of beta-lactams: initial bacteriological characterization. Antimicro Agents Chemother 1978; 14: 414-9.
16. Aronoff SC, Jacobs MR, Johenning S, Yamabe S. Comparative activities of the beta-lactamase inhibitors YTR 830, sodium clavulanate, and sulbactam combined with amoxicillin or ampicillin. Antimicro Agents Chemother 1984; 26: 580-2.
17. Ambler RP. The amino acid sequence of Staphylococcus aureus penicillinase. Biochem J 1975; 151: 197-218.
18. Meadway RJ. The amino acid sequence of penicillinase from Bacillus licheniformis. Biochem J 1969; 115: 12-3.
19. Frère JM, Duez C, Ghuysen JM, Vandekerckhove J. Occurrence of a serine residue in the penicillin-binding site of the exocellular DDcarboxypeptidase- transpeptidase from Streptomyces R61. FEBS Lett 1976; 70: 257-60.
20. Knott-Hunziker V, Waley SG, Orlek BS, Sammes PG. Penicillinase active sites: labeling of serine-44 in beta-lactamase I by 6 beta-bromopenicillanic acid. FEBS Lett 1979; 99: 59-61.
21. Ambler RP, Coulson AFW, Frère JM, et al. A standard numbering scheme for the Class A beta-lactamases. Biochem J 1991; 276: 269-72.
22. Fisher J, Belasco JG, Charnas RL, Khosla S, Knowles JR. Betalactamase inactivation by mechanism-based reagents. Philos Trans R Soc Lond B Biol Sci 1980; 289: 309-19.
23. Fisher J, Belasco JG, Khosla S, Knowles JR. Beta-lactamase proceeds via an acyl-enzyme intermediate. Interaction of the Escherichia coli RTEM enzyme with cefoxitin. Biochemistry 1980; 19: 2895-901.
24. Galleni M, Frère JM. A survey of the kinetic parameters of class C beta-lactamases. Penicillins. Biochem J 1988; 255: 119-22.
25. Galleni M, Amicosante G, Frère JM. A survey of the kinetic parameters of class C beta-lactamases. II. Cephalosporins and other beta-lactam compounds. Biochem J 1988; 255: 123-29.
26. Bengtåke J, Grundström T. ampC cephalosporinase of Escherichia coli K-12 has a different evolutionary origin from that of betalactamases of the penicillinase type. Proc Natl Acad Sci USA 1981; 78: 4897-901.
27. Huovinen P, Huovinen S, Jacoby GA. Sequence of PSE-2 betalactamase. J Antimicrob Chemother 1988; 32: 134-6.
28. Frère JM. Beta-lactamases. (Molecular anatomy and physiology of proteins). New York: Nova Science Publishers 2012.
29. Kelly JA, Moews PC, Knox JR, Frère JM, Ghuysen JM. Structure of a penicillin target enzyme and location of the antibiotic binding site. Science 1982; 218: 479-80.
30. Samraoui B, Sutton BJ, Todd RJ, Artymiuk PJ, WaleySG, Phillips DC. Tertiary structural similarity between a class A beta-lactamase and a penicillin-sensitive D-alanyl carboxypepetidase-transpeptidase. Nature 1986; 320: 378-80.
31. Tipper DJ, Strominger JL. Mechanisms of action of pencillins: a proposal based on their structural similarity to acyl-D-alanyl-Dalanine. Proc Natl Acad Sci USA 1965; 54: 1133-41.
32. Bush K. Excitement in the beta-lactamase arena. J Antimicrob Chemother 1989; 24: 831-40.
33. Sirot D, Sirot J, Labia R, et al. Transferable resistance to thirdgeneration cephalosporins in clinical isolates of Klebsiella pneumonia: identification of CTX-1, a novel beta-lactamase. J Antimicrob Chemother 1987; 20: 323-34.
34. Nordmann P, Ronco E, Naas T, Duport C, Michel-Briand Y, Labia R. Characterization of a novel extended-spectrum beta-lactamase from Pseudomonos aeruginosa. Antimicro Agents Chemother 1993; 37: 962-9.
35. Bauernfeind A, Stemplinger I, Jungwirth R, Ernst S, Casellas JM. Sequences of beta-lactamase genes encoding CTX-M-1 (MEN-1) and CTX-M-2 and relationship of their amino acid sequences with those of other beta-lactamases. Antimicro Agents Chemother 1996; 40: 509-13.
36. Thomson KS, Weber DA, Sanders CC, Sanders WE JR. Betalactamase production in members of the family Enterobacteriaceae and resistance to beta-lactam enzyme inhibitor combinations. Antimicro Agents Chemother 1990; 34: 622-7.
37. Kahan JS, Kahan FM, Goegelman RC, et al. Thienamycin, a new beta-lactam antibiotic. Discovery, taxonomy, isolation and physical properties. J Antibiotic 1979; 32: 1-12.
38. Christensen BG, Leanza WJ, Wildonger KJ. Substituted Nmethylene derivatives of thienamycin. United States Patent 4,194,047 1980.
39. Clissold SP, Todd PA, Campoli-Richards DM. Imipenem/cilastatin. A review of its antibacterial activity, pharmacokinetic properties and therapeutic efficacy. Drugs 1987; 33: 183-241.
40. Edwards JR, Turner PJ, Wannop C, Withnell ES, Grindey AJ, Nairn K. In vitro antibacterial activity of SM-7338, a carbapenem antibiotic with stability to dehydropeptidase I. Antimicrob Agents Chemother 1989; 33: 215-22.
41. Queenan AM, Bush K. Carbapenemases: the versatile betalactamases. Clin Microbiol Rev 2007; 20: 440-58.
42. Walsh TR. Clinically significant carbapenemases: an update. Curr Opin Infect Dis 2008; 21: 367-71.
43. Yang Y, Wu P, Livermore DM. Biochemical characterization of a beta-lactamase that hydrolyzes penems and carbapenems from two Serratia marcescens isolates. Antimicrob Agents Chemother 1990; 34: 755-8.
44. Naas T, Vandel L, Sougakoff W, Livermore DM, Nordmann P. Cloning and sequence analysis of the gene for a carbapenemhydrolyzing class A beta-lactamase, Sme-1, from Serratia marcescens S6. Antimicrob Agents Chemother 1994; 38: 1262-70.
45. Nordmann P, Mariotte S, Naas T, Labia R, Nicolas MH. Biochemical properties of a carbapenem-hydrolyzing beta-lactamas from Enterobacter cloacae and cloning of the gene into Escherichia coli. Antimicrob Agents Chemother 1993; 37: 939-46.
46. Naas T, Nordmann P. Analysis of a carbapenem-hydrolyzing class A beta-lactamase from Enterobacter cloacae and of its LysR-type regulatory protein. Proc Natl Acad Sci USA 1994; 91: 7693-97.
47. Raquet X, Lamotte-Brasseur J, Bouillenne F, Frère JM. A disulfide bridge near the active site of carbapenem-hydrolyzing class A betalactamase might explain their unusuel substrate profile. Proteins 1997; 27: 47-58.
48. Swarén P, Maveyraud L, Raquet X, et al. X-ray analysis of the NMC-A beta-lactamase at 1.64-Å resolution, a class A carbapenemase with broad substrate specificity. J Biol Chem 1998; 273: 26714-21.
49. Yigit H, Queenan AM, Anderson GJ, et al. Novel carbapenemhydrolyzing beta-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsellia pneumonia. Antimicrob Agents Chemother 2001; 45: 1151-61.
50. Walther-Rasmussen J, Høiby. Class A carbapenemases. J. Antimicrob Chemother 2007; 60: 470-82.
51. Ke W, Bethel CR, Thomson JM, Bonomo RA, van den Akker F. Crystal structure of KPC-2: insights into carbapenemase activity in class A beta-lactamase. Biochemistry 2007; 46: 5732-40.
52. Smith CA, Caccamo M, Kantardjieff KA, Vakulenko S. Structure of GES-1 at atomic resolution: insights into the evolution of carbapenemase activity in the class A extended-spectrum betalactamases. Acta Cryst 2007; D63: 982-92.
53. Smith CA, Frase H, Toth M, et al. Structural basis for progression toward the carbapenemase activityin the GES family of betalactamase. J Am Chem Soc 2012; 134: 19512-5.
54. Delbrück H, Bogaerts P, Kupper MB, et al. Kinetic and crystallography studies of extended-spectrum GES-11, GES-12, and GES-14 beta-lactamases. Antimicrob Agents Chemother 2012; 56: 5618-25.
55. Abrahm EP, Newton GGF. Experiments on the degradation of cephalosporin C. Biochem J 1956; 62: 658-65.
56. Sabath LD, Abraham EP. Zinc as a cofactor for cephalosporinase from Bacillus cereus 569. Biochem J 1966; 98: 11c.
57. Kuwabara S, Abraham EP. Some properties of two extracellular beta-lactamases from Bacillus cereus 569H. Biochem J 167; 103: 27c.
58. Lim HM, Pène JJ, Shaw RW. Cloning, nucleotide sequence, and expression of the Bacillus cereus 5/B/6 beta-lactamase II structural gene. J Bacteriol 1988; 170: 2873-8.
59. Hussain M, Carlino A, Madonna MJ, Lampen JO. Cloning and sequencing of the metallthioprotein beta-lactamase II gene of Bacillus cereus 569/H in Escherichia coli. J Bacteriol 1985; 164: 223- 9.
60. Felici A, Amicosante G, Oratore A, et al. An overview of the kinetic parameters of class B beta-lactamases. Biochem J 1993; 291: 151-5.
61. Saino Y, Kobayashi F, Inoue M, Mitsuhashi S. Purification and properties of inducible penicillin beta-lactamase isolated from Pseudomonas maltophilia. Antimicrob Agents Chemother 1982; 22: 564-70.
62. Cuchural GJ Jr. Malamy MH, Tally FP. Beta-lactamase-mediated imipenem resistance in Bacteroides fragilis. Antimicrob Agents Chemother 1986; 30: 645-8.
63. Rasmussen BA, Gluzman Y, Tally FP. Cloning and sequencing of the class B beta-lactamase gene (ccrA) from Bacteroides fragilis TAL3636. Antimicrob Agents Chemother 1990; 34: 1590-2.
64. Walsh TR, Hall L, Assinder SJ, et al. Sequence analysis of the L1 metallo-beta-lactamase from Xanthomonas maltophilia. Biochim Biophys Acta 1994; 1218: 199-201.
65. Iaconis JP, Sanders CC. Purification and characterization of inducible beta-lactamase in Aeromonas spp. Antimicrob Agents Chemother 1990; 34: 44-51.
66. Massidda O, Rossolini GM, Satta G. The Aeromonas hydrophila cphA gene: molecular heterogeneity among class B metallo-betalactamase. J Bacteriol 1991; 173: 4611-7.
67. Bebrone C, Garau G, Garcia-Saez I, Chantalat L, Carfi A, Dideberg O. X-ray structures and mechanisms of metallo-beta-lactamase. In: Frère JM, Ed. Beta-lactamases. New York: Nova Science Publishers 2012.
68. Carfi A, Pares S, Duée E, et al. The 3-D structure of a zinc metallobeta- lactamase from Bacillus cereus reveals a new type of protein fold. EMBO J 1995; 14: 4914-21.
69. Concha NO, Rasmussen BA, Bush K, Herzberg O. Crystal structure of the wide-spectrum binuclear zinc beta-lactamase from Bacteroides fragilis. Structure 1996; 4: 823-36.
70. Carfi A, Duée E, Galleni M, Frère JM, Dideberg O. 1.85 Á resolution structure of the Zinc(II) beta-lactamase from Bacillus cereus. Acta Cryst 1998; D54: 313-23.
71. Garau G, Bebrone C, Anne C, Galleni M, Frère JM, Dideberg O. A metallo-beta-lactamase enzyme in action: crystal structure of the monozinc carbapenemase CphA and its complex with biapenem. J Mol Biol 2005; 345: 785-95.
72. Ullah JH, Walsh TR, Taylor IA, et al. The crystal structure of the L1 metallo-beta-lactamase from Stenotrophomonas maltophilia at 1.7 Å resolution. J Mol Biol 1998; 284: 125-36.
73. Morán-Barrio J, González JM, Lisa MN, et al. The metallo-betalactamase GOB is a mono-Zn (II) enzyme with a novel active site. J Biol Chem 2007; 282: 18286-93.
74. Watanabe M, Iyobe S, Inoue M, Mitsuhashi S. Transferable imipenem resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 1991; 35: 147-51.
75. Laraki N, Franceschini N, Rossolini GM, et al. Biochemical characterization of the Pseudomonas aeruginosa 101/1477 metallobeta- lactamase IMP-1 produced by Escherichia coli. Antimicrob Agents Chemother 1999; 43: 902-6.
76. Osano E, Arakawa Y, Wacharotayankun R, et al. Molecualr characterization of an enterobacterial metallo-beta-lactamase found in a clinical isolate of Serratia marcescens that shows imipenem resistance. Antimicrob Agents Chemother 1994; 38: 71-78.
77. VIM; a new integron-borne metallo-beta-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob Agents Chemother 1999; 43: 1584-90.
78. NDM-1 and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother 2009; 53: 5046-54.
79. Zhang HM, Hao Q. Crystal structure of NDM-1 reveals a common beta-lactam hydrolysis mechanism. FASEB J 2011; 25: 2574-82.
80. King D, Strynadka N. Crystal structure of New Delhi metallo-betalactamase reveals molecular basis for antibiotic resistance. Protein Sci 2011; 20: 1484-91.
81. Leski T, Vora GJ, Taitt CR. Multidrug resistance determinants from NDM-1-producing Klebsiella pneumonia in the USA. Int J Antimicrob Agents 2012; 40: 282-4.
82. Lakaye B, Dubus A, Lepage S, Groslambert S, Frère JM. When drug inactivation renders the target irrelevant to antibiotic resistance: a case story with beta-lactams. Mol Microbiol 1999; 31: 89- 101.
83. Masuda N, Sakagawa E, Ohya S, Gotoh N, Tsujimoto H, Nishino T. Substrate specificities of MexAB-OprM, MexCD-OprJ, and MexXY-OprM efflux pumps in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2000; 44: 3322-7.
84. Quale J, Bratu S, Gupta J, Landman D. Interplay of efflux system, ampC, and oprD expression in carbapenem resistance of Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother 2006; 50: 1633-41.
85. Wouters J, Bauvois C. Structure of class C beta-lactamases and perspectives in drug design. In: JM Frère, Ed. Beta-lactamases. New York: Nova Science Publishers 2012; pp. 79-102.
86. Nordmann P, Poirel L. Emerging carbapenemases in Gramnegative aerobes. Clin Microbiol Infect 2002; 8: 321-31.
87. Donald HM, Scaife W, Amyes SG, Young HK. Sequence analysis of ARI-1, a novel OXA beta-lactamase, responsible for imipenem resistance in Acinetobacter baumannii 6B92. Antimicrob Agents Chemother 2000; 44: 196-9.
88. Afzal-Shah M, Woodford N, Livermore DM. Characterization of OXA-25, OXA-26, and OXA-27, molecular class D betalactamases associated with carbapenem resistance in clinical isolates of Acinetobacter baumannii. Antimicrob Agents Chemother 2001; 45: 583-8.
89. Paton R, Miles RS, Hood J, Amyes SG, Miles RS, Amyes SG. ARI-1: beta-lactamase-mediated imipenem resistance in Acinetobacter baumannii. Antimicrob Agents Chemother 1993; 2: 81-7.
90. Poirel L, Héritier C, Tolün V, Nordmann P. Emergence of oxacillinase- mediated resistance to imipenem in Klebsiella pneumonia. Antimicrob Agents Chemother 2004; 48: 15-22.
91. Poirel L, Castanheira M, Carrër A, et al. OXA-163, an OXA-48- related class D beta-lactamase with extended activity toward expanded- spectrum cephalosporins. Antimicrob Agents Chemother 2011; 55: 2546-51.
92. Walther-Rasmussen J, Høiby N. OXA-type carbapenemases. J Antimicrob Chemother 2006; 57: 373-83.
93. Kerff F, Sauvage E, Vercheval L, Charlier P. In: Beta-lactamases; Frère JM, Ed. NewYork: Nova Science Publishers 2012; pp. 103-8.
94. Ehmann DE, Jahić H, Ross PL, et al. Avibactam is a covalent, reversible, non-beta-lactam beta-lactamase inhibitor. PNAS 2012; 109: 11663-88.
95. Ehmann DE, Jahić H, Ross PL, et al. Kinetics of avibactam inhibition against class A, C and D beta-lactamases. J Biol Chem 2013; 288: 27960-71.
96. King AM, Reid-Yu SA, Wang W, et al. Aspergillomarasmine A overcomes metallo-beta-lactamase antibiotic resistance. Nature 2014; 510: 503-6.
97. Laraki N, Franceschini N, Rossolini GM, et al. Biochemical characterization of the Pseudomonas aeruginosa 101/1477 metallobeta- lactamase IMP-1 produced by Escherichia coli. Antimicrob Agents Chemother 1999; 43: 902-6.
98. Docquier JD, Lamotte-Brasseur J, Galleni M, Amicosante G, Frère JM, Rossolini GM. On functional and structural heterogeneity of VIM-type metallo-beta-lactamases. J Antimicrob Chemother 2003; 51: 257-66.
99. Thomas PW, Zheng M, Wu S, et al. Characterization of purified New-Delhi metallo-beta-lactamase-1. Biochemistry 2011; 50: 10102- 13.