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Antimicrobial Agents and Chemotherapy, August 2001, p. 2368-2371, Vol. 45, No. 8
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.8.2368-2371.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Identification of a Plasmid Encoding SHV-12, TEM-1,
and a Variant of IMP-2 Metallo-
-Lactamase, IMP-8, from a
Clinical Isolate of Klebsiella pneumoniae
Jing-Jou
Yan,1
Wen-Chien
Ko,2 and
Jiunn-Jong
Wu3,*
Departments of
Pathology1 and
Medicine,2 National Cheng Kung
University Medical Center, and Department of Medical
Technology,3 National Cheng Kung University
Medical College, Tainan, Taiwan
Received 7 December 2000/Returned for modification 20 March
2001/Accepted 11 May 2001
 |
ABSTRACT |
A multidrug-resistant plasmid encoding TEM-1, SHV-12, and a variant
of IMP-2 metallo-
-lactamase, designated IMP-8, was identified from a
clinical isolate of Klebsiella pneumoniae. There are four nucleotide differences between blaIMP-2 and
blaIMP-8, resulting in two amino acid
differences. blaIMP-8 was also found to be
carried by an integron-borne gene cassette similar to the
blaIMP-2 cassette.
| |
TEXT |
The emergence of
carbapenem-hydrolyzing metallo--lactamases in gram-negative bacteria
has raised serious concern, since the enzymes usually possess a broad
hydrolysis profile that includes carbapenems and extended-spectrum
-lactams (6, 8, 12, 13, 15). The genetic determinants
of the metallo--lactamases are usually carried on mobile gene
cassettes inserted in plasmid- or chromosome-borne integrons (1,
8, 13, 15). Since 1991, the IMP-1 metallo--lactamase has
spread among isolates of various members of the family
Enterobacteriaceae, Pseudomonas aeruginosa, and other
nonfastidious, gram-negative nonfermenters in Japan (5, 6, 17,
18). Several novel metallo--lactamases have been described
more recently. VIM-1 and VIM-2 were found to be produced by P. aeruginosa isolates from Italy (8) and France
(13), respectively. IMP-2 was detected in an Italian isolate of Acinetobacter baumannii and was chromosomally
encoded (15). IMP-3 was detected in a Shigella
flexneri isolate in Japan and was plasmid mediated
(7). Among these metallo--lactamases, only IMP-1 has
been described in Klebsiella pneumoniae in Japan (5) and Singapore (T. H. Koh, G. S. Babini, N. Woodford, L.-H. Sng, L. M. C. Hall, and D. M. Livermore, Letter, Lancet 353: 2162, 1999). In this report
we describe a plasmid encoding TEM-1, the SHV-12 extended-spectrum
-lactamase, and a variant of the IMP-2 enzyme (designated IMP-8)
from a clinical isolate of K. pneumoniae.
Bacterial strains and vectors.
K. pneumoniae KPO787
was recovered from a central venous catheter tip that was removed from
a patient with diabetes mellitus and acute pancreatitis at the
intensive care unit of the National Cheng Kung University Medical
Center in 1998. The isolate could be a colonizer, and the patient died
of multiple organ system failure unrelated to the infection after 40 days of hospitalization. The recipient strain was Escherichia
coli C600 (2), which is resistant to streptomycin.
E. coli HB101 was the host for the cloning experiments
(16). An E. coli C600 strain carrying a blaSHV-12-containing plasmid (pEKPB657) that was
transferred from a clinical isolate of K. pneumoniae was
used for comparison in susceptibility tests (20). The
cloning vectors used were pUC19 and pHP13 (4, 21). pHP13
is a bifunctional multicopy vector with erythromycin and
chloramphenicol-resistance markers (4).
Susceptibility tests.
MICs of antimicrobial agents were
determined by the agar dilution method according to the guidelines of
the National Committee for Clinical Laboratory Standards
(11). The antibiotics used in the study were obtained from
the following sources: amoxicillin, SmithKline Beecham Pharmaceuticals,
Surrey, United Kingdom; aztreonam, Bristol-Myers Squibb, New Brunswick,
N.J.; cefotaxime and cefuroxime, Hoechst-Roussel Pharmaceuticals, Inc.,
Somerville, N.J.; ceftazidime, Glaxo Group Research, Ltd., Greenford,
United Kingdom; ceftriaxone, Hoffmann-La Roche, Inc., Nutley, N.J.;
cefoxitin and imipenem, Merck Sharp & Dohme, West Point, Pa.;
meropenem, Sumitomo Pharmaceuticals, Ltd., Osaka, Japan; cephalothin
and cefaclor, Eli Lilly & Co., Indianapolis, Ind.; piperacillin,
Lederle Laboratories, Pearl River, N.Y.; and streptomycin and
chloramphenicol, Sigma Chemical Co., St. Louis, Mo.
Transfer of resistance determinants.
Conjugation experiments
were performed by broth mating as described previously (14,
20). Transconjugants were selected on tryptic soy agar plates
supplemented with streptomycin (500 µg/ml) and ceftazidime (10 µg/ml).
Plasmid DNA preparation.
Plasmid preparation was performed by
the rapid alkaline lysis method (19). Plasmid DNA obtained
from the transconjugant was restricted with EcoRI or
PstI (Roche Molecular Biochemicals, Mannheim, Germany), and
its size was estimated by adding up the restriction fragment lengths.
Detection of the blaSHV and
blaTEM genes.
PCR was used to amplify the
entire sequences of the blaSHV and
blaTEM genes in plasmid preparations as
described previously (20). The amplicons were purified
with PCR clean up kits (Roche Molecular Biochemicals) and were
sequenced on an ABI PRISM 377 sequencer analyzer (Applied Biosystems,
Foster City, Calif.).
Cloning and sequencing of the blaIMP-8
gene.
The resistance plasmid (pEKPO787) obtained from the
transconjugant was digested with PstI. A 5.6-kb fragment was
cloned into vector pUC19 (pEKPO787-1). The insert was further digested
with BamHI and KpnI, and a 1.9-kb fragment was
subcloned into vector pUC19 (pEKPO787D). Since there is no
KpnI site on pHP13, a 1.9-kb BamHI-EcoRI fragment, which included the 1.9-kb
BamHI-KpnI insert and the EcoRI site
of pUC19, from pEKPO787D, was further ligated to pHP13, giving rise to
pEKPO787D1. The insert was sequenced. Nucleotide and derived amino acid
sequences were analyzed with the GCG program (Genetics Computer Group,
Inc., Madison, Wis.). Related -lactamases were identified by
comparison with the GenBank and SWISS-PROT databases.
Isoelectric focusing of -lactamases.
Crude homogenates of
-lactamases were prepared as described previously (3).
Isoelectric focusing analysis was performed by the method of Matthew et
al. (10) as described previously (20).
An approximately 150-kb plasmid was successfully transferred from
K. pneumoniae KPO787 to E. coli C600. PCR and
sequence analyses showed that both the clinical isolate and its
transconjugant carried SHV-12 and TEM-1.
The nucleotide sequence of a 1.9-kb fragment cloned into vector pUC19
and pHP13 contained an open reading frame of 741 nucleotides
which
corresponded to a putative protein of 246 amino acids (Fig.
1). The sequence of the gene is identical
to that of
blaIMP-2,
except for four nucleotide
substitutions which resulted in two
amino acid changes. Substitutions
of a G for a C and a C for a
G at nucleotide positions 61 and 62, respectively, and substitution
of a G for a T at nucleotide position
617 resulted in the replacements
of an Arg by an Ala and a Val by a Gly
at amino acid positions
21 and 206, respectively, in the mature
metallo-
-lactamase. The
blaIMP-2-related
gene, now designated
blaIMP-8, was found to be
flanked by nucleotide sequences identical to partial sequences
of the
intII and
aac(6')Ib genes (Fig.
1), indicating
that
blaIMP-8 is also carried on an
integron-borne gene cassette.
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FIG. 1.
Nucleotide sequence of the
blaIMP-8 gene and flanking regions. The deduced
amino acid sequence of blaIMP-8 is indicated in
the single-letter code below the nucleotide sequence of
blaIMP-8. The start codons of intII,
blaIMP-8, and aac(6')Ib are indicated by
horizontal arrows, and the stop codon of
blaIMP-8 is indicated by three asterisks. The
nucleotides and amino acids that differ between
blaIMP-8 and blaIMP-2 are
marked by bold letters, and the nucleotides and amino acids for
blaIMP-2 and IMP-2 that differ from the
sequences for blaIMP-8 and IMP-8 are shown above
and below the sequences. The blaIMP-8 cassette
boundaries are indicated by vertical arrows. The conserved core and
inverse core sites located at the blaIMP-8
cassette boundaries are boxed.
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|
Isoelectric focusing revealed production of
-lactamases with pIs of
5.4, 7.6, and 8.2 by
K. pneumoniae KPO787 (Fig.
2). The
-lactamases with pIs of 5.4 and 8.2 were transferred to
E. coli C600. Thus, the pI 7.6 band probably represented the chromosomal
SHV-1
-lactamase of the
K. pneumoniae strain (
9). The
E. coli HB101 strain transformed by pEKPO787D1 had a pI 8.2 band
only,
indicating that the pI of IMP-8 is 8.2, as is that of SHV-12.
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|
FIG. 2.
Results of isoelectric focusing analysis. Lane 1, K. pneumoniae KPO787; lane 2, E. coli
C600(pEKPO787); lane 3, E. coli HB101(pEKPO787D1); lane 4, K. pneumoniae KPT986, a clinical isolate known to produce
TEM-1 (pI 5.4), SHV-1 (pI 7.6), and SHV-12 (pI 8.2) (18).
The numbers on the right are pIs.
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|
The susceptibilities of
K. pneumoniae KPO787, its
transconjugant, and the transformant
E. coli HB101 to
various
-lactams
are shown in Table
1.
Compared with the quality control strain
E. coli ATCC 25922 (
11), the
K. pneumoniae strain showed increased
resistance to imipenem (MIC, 0.25 versus 8 µg/ml) and meropenem
(MIC,
0.06 versus 16 µg/ml) and high-level resistance to all the
other
-lactam agents tested. The resistance phenotype of the
transconjugant is quite similar to that of the clinical isolate,
except
that the MICs of carbapenems were relatively low for the
transconjugant, as was expected from previous findings
(
6).
Unlike the clinical strain and its transconjugant,
the transformant
showed susceptibility to aztreonam.
IMP-2 was first reported on the chromosome of an
A. baumannii strain in Italy (
15). The
blaIMP-2 gene shares an 88% nucleotide
identity
with
blaIMP-1 and is carried by a gene cassette
unrelated
to the
blaIMP-1 cassette. The
blaIMP-8 gene found in this study
is very
closely related to
blaIMP-2, with only four
nucleotide
differences from
blaIMP-2.
blaIMP-8 was also found to be carried
by a gene
cassette related to the
blaIMP-2 cassette;
however,
in contrast to the
blaIMP-2 cassette,
the
blaIMP-8 cassette was
located on the
plasmid, which would facilitate the spread of the
resistance
gene.
Production of IMP-8 in the
E. coli transformant caused
reduced susceptibilities to almost all
-lactams, including
penicillins,
cephalosporins, and carbapenems. Only aztreonam was
unaffected,
in agreement with the properties of other
metallo-
-lactamases
(
6,
8,
12,
13,
15). Resistance to
aztreonam in the
K. pneumoniae isolate and its
transconjugant should be due to
the effects of SHV-12, the most
prevalent type of extended-spectrum
-lactamase among clinical
isolates of
K. pneumoniae at the National
Cheng Kung Medical
Center (
20). The
blaIMP-8
containing integron
was also found to carry an aminoglycoside
resistance gene,
aac(6')Ib.
Thus, antibiotics that can be
used to treat infections with the
microorganisms containing this
multidrug-resistant plasmid are
very limited. Since
K. pneumoniae is a notorious host of resistance
plasmids, the
prevention of the spread of the multidrug-resistant
plasmid and strain
is critical and has become a big challenge
to the hospital
staff.
Nucleotide sequence accession number.
The nucleotide sequence
data reported in this paper have been submitted to GenBank and assigned
accession no. AF322577.
| |
ACKNOWLEDGMENTS |
This work was partially supported by grants NCKUH89-054 from
National Cheng Kung University Hospital and NSC89-2320-B-006-149 from
the National Science Council, Republic of China.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Medical Technology, National Cheng Kung University Medical College, 1 University Rd., Tainan, Taiwan 70101. Phone: 886-6-2353535, ext. 5775. Fax: 886-6-2363956. E-mail: jjwu{at}mail.ncku.edu.tw.
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Antimicrobial Agents and Chemotherapy, August 2001, p. 2368-2371, Vol. 45, No. 8
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.8.2368-2371.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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