Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AAC
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • AAC Podcast
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Antimicrobial Agents and Chemotherapy
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AAC
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • AAC Podcast
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Minireview

Nomenclature for Macrolide and Macrolide-Lincosamide-Streptogramin B Resistance Determinants

Marilyn C. Roberts, Joyce Sutcliffe, Patrice Courvalin, Lars Bogo Jensen, Julian Rood, Helena Seppala
Marilyn C. Roberts
Department of Pathobiology, University of Washington, Seattle, Washington 98195;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Joyce Sutcliffe
Department of Infectious Diseases, Pfizer Central Research, Groton, Connecticut 06340-1596;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Patrice Courvalin
Unite des Agents Antibacterienes, Institute Pasteur, Paris Cedex 15, France;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lars Bogo Jensen
Danish Veterinary Laboratory, DK-1790 Copenhagen, Denmark;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Julian Rood
Department of Microbiology, Monash University, Clayton, Victoria 3168, Australia; and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Helena Seppala
Antimicrobial Research Laboratory, National Public Health Institute, FIN-20520 Turku, Finland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/AAC.43.12.2823
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

Macrolides are composed of 14 (erythromycin and clarithromycin)-, 15 (azithromycin)-, or 16 (josamycin, spiramycin, and tylosin)-membered lactones to which are attached amino and/or neutral sugars via glycosidic bonds. Erythromycin was introduced in 1952 as the first macrolide antibiotic. Unfortunately, within a year, erythromycin-resistant (Emr) staphylococci from the United States, Europe, and Japan were described (101). Erythromycin is produced bySaccharopolyspora erythraea, while the newer macrolides are semisynthetic molecules with substitutions on the lactone. The newer derivatives, such as clarithromycin and azithromycin, have improved intracellular and tissue penetration, are more stable, are better absorbed, have a lower incidence of gastrointestinal side effects, and are less likely to interact with other drugs. They are useable against a wider range of infectious bacteria, such as Legionella, Chlamydia,Haemophilus, and some Mycobacterium species (notM. tuberculosis), and their pharmacokinetics provide for less frequent dosing than erythromycin (21, 47, 96, 97). As a result, the usage of the newer macrolides has increased dramatically over the last few years, which has led to increased exposure of bacterial populations to macrolides (101-103, 107).

Macrolides inhibit protein synthesis by stimulating dissociation of the peptidyl-tRNA molecule from the ribosomes during elongation (101, 103). This results in chain termination and a reversible stoppage of protein synthesis. The first mechanism of macrolide resistance described was due to posttranscriptional modification of the 23S rRNA by the adenine-N6 methyltransferase (101-103). These enzymes add one or two methyl groups to a single adenine (A2058 in Escherichia coli) in the 23S rRNA moiety. Over the last 30 years, a number of adenine-N6-methyltransferases from different species, genera, and isolates have been described. In general, genes encoding these methylases have been designated erm(erythromycin ribosome methylation), although there are exceptions, especially in the antibiotic-producing organisms (see Tables 1 and 3) (103). As the number of erm genes described has grown, the nomenclature for these genes has varied and has been inconsistent (Table 1). In some cases, unrelated genes have been given the same letter designation, while in other cases, highly related genes (>90% identity) have been given different names.

View this table:
  • View inline
  • View popup
Table 1.

rRNA methylase genes involved in MLSB resistance

The binding site in the 50S ribosomal subunit for erythromycin overlaps the binding site of the newer macrolides, as well as the structurally unrelated lincosamides and streptogramin B antibiotics. The modification by methylase(s) reduces the binding of all three classes of antibiotics, which results in resistance against macrolides, lincosamides, and streptogramin B antibiotics (MLSB). The rRNA methylases are the best studied among macrolide resistance mechanisms (47, 101-103). However, a variety of other mechanisms have been described which also confer resistance (Table2). Many of these alternative mechanisms of resistance confer resistance to only one or two of the antibiotic classes of the MLSB complex.

View this table:
  • View inline
  • View popup
Table 2.

Efflux and inactivating genes

In this review, we suggest a new nomenclature for naming MLS genes and propose to use the rules developed for identifying and naming new tetracycline resistance genes (51, 52). This system, with a few recent modifications, was originally designed because of the ability of two genes to be distinguished uniquely by DNA-DNA probe methodology (51). It was generally found that two genes with <80% amino acid sequence identity provided enough variability in nucleotide sequence to permit distinct probes to be designed. Although many investigators are likely to sequence new genes, the use of probe technology allows rapid identification of isolates containing potentially new genes, as well as a reliable way to screen populations and determine the frequency of any one resistant determinant. Therefore, we continued this paradigm by assigning two genes of ≥80% amino acid identity to the same class and same letter designation, while two genes that show ≤79% amino acid identity are given a different letter designation. Table 1 shows the results of the classification, with some classes having members with little variability, while others, like classes A and O, show a greater range of homology at both the DNA and amino acid levels. As new gene sequences emerge, ideally they will need to be compared by oligonucleotide probe hybridization and/or sequence analysis against the bank of known genes before a new designation is assigned. If multiple genes are available in any one class, especially when there is a range as in class A, then all representative members of the class should be examined, not just one. To confirm that the proposed name or number for the newly discovered resistance determinant has not been used by another investigator, please contact M. C. Roberts for this information. A similar request has been made for newtet genes (52).

RRNA METHYLASES

Over the last 30 years, a large number of different rRNA methylase genes (erm) have been isolated from a variety of bacteria that range from E. coli to Haemophilus influenzaein gram-negative species and from Streptococcus pneumoniaeto Corynebacterium spp. in gram-positive species (Table3). In addition, a variety of gram-positive and gram-negative anaerobes, and even spirochetes such as Borrelia burgdorferi and Treponema denticola, have all been shown to carry erm genes (Table 3) (36, 77, 78). All erm enzymes methylate the same adenine residue, resulting in an MLSB phenotype (9, 100-103). This adenine (A2058) or one of the adjacent residues in the peptidyltransferase region (A2057 or A2059) is changed to another nucleotide by mutation in macrolide-resistant Mycobacterium intracellulare,Mycobacterium avium, Propionibacterium spp., andHelicobacter pylori (58, 84, 100-103).

View this table:
  • View inline
  • View popup
Table 3.

Location of antibiotic resistance genesa

Differences between the various erm genes are seen in the regulation of expression of the phenotype. Some of the enzymes are inducibly regulated by translational attenuation of a mRNA leader sequence; in the absence of erythromycin, the mRNA is in an inactive conformation due to a sequestered Shine-Dalgarno sequence, preventing efficient initiation of translation of theerm transcripts. Mutational analyses of theerm(C) leader peptide suggested that the peptide, (FS)IFVI, is critical for induction (103). However, when theerm peptides from the erm genes are compared, little sequence similarity is apparent (103). Recently, a second mechanism of regulation has been described in which the lack of erythromycin prevents the complete synthesis of the mRNA due to rho factor-independent termination. This type of regulation has been described for the erm(K) system (20), and by homology, we hypothesize that it may also exist for erm(D), as well as erm(J), because they are highly related and have been grouped together under class D (Table 1). In either system, inducible isolates, when tested, may appear to be susceptible or intermediately resistant to macrolides and susceptible to lincosamides. Erythromycin is generally a good inducer in most species; in animal or human streptococcal isolates, lincosamides and/or streptogramin B may be good inducers (47, 76). Good overviews of regulation of the erm genes can be found in recent reviews by Weisblum (100-103).

Inducible strains predominated in the 1960s to 1970s. However, today it is more common in many geographical areas to find isolates that constitutively produce the rRNA methylase without preexposure to antibiotics. Constitutive erm gene expression is usually associated with structural alterations in the ermtranslational attenuator, including deletions, duplications, and point mutations in erm(C) (104). They can be distinguished from inducible isolates by the stable MICs for them regardless of whether they are pregrown with or without an inducer (76, 102).

Many of the erm genes are associated with conjugative or nonconjugative transposons which tend to reside on the chromosomes, although some have been found in plasmids. They are often associated with other antibiotic resistance genes, especially tetracycline resistance genes. The erm(F) gene is often linked with thetet(Q) gene, while the erm(B) gene is often linked with the tet(M) gene (24, 86, 95). These conjugative transposons can have a wide host range, which may explain why clinical isolates of many different bacterial species have been found to carry these erm genes (Table 3). The ermgenes in general have low G+C contents (31 to 34%), while the overall chromosomal G+C contents found in gram-negative species are ≥50% and ∼35% in gram-positive species.

It has been common practice for investigators to give theirerm gene a new name regardless of the DNA and predicted amino acid sequence similarity to previously characterizederm genes and without regard to whether the gene resides in a different isolate, species, or genus. The result has been that, over the years, the names of these erm genes have become confusing, and often a complex table is required to remember which genes are closely related (Table 1). In the worst cases, genes for unrelated enzymes have been given the same name (erm(A), causing confusion in the literature and GenBank listings (Table 1). The opposite also has occurred where very closely related or virtually identical enzymes have been given a variety of different names. For example, erm(F) (GenBank no. M14730) is found on theBacteroides transposons Tn4351 and Tn4000 (71), erm(FS) (no. M17808) is on Bacteroides transposon Tn4551 (91), and erm(FU) (no. M62487) (32) is also fromBacteriodes. All three enzymes share ≥97% DNA and amino acid identity (Table 1). Since there are no phenotypic differences between the three erm(F) genes and distinguishing them by any method other than sequencing is problematic, we propose that all three should be known as class F: the Erm(F) protein and theerm(F) gene (Table 1).

The situation is even worse with class B, which is composed of a larger number of genes, including erm(AM), erm(B),erm(BC), erm(BP), and erm(Z), whose sequences share ≥98% homology (Table 1). Because the normal gene designation is to use a single letter (26) and the possibility of confusion between erm(A) anderm(AM), we propose that this group be known as class B: theerm(B) genes and the Erm(B) protein (Table 1). Recent dendrograms of many of the erm genes can be found in articles by Seppälä et al. (88) and Matsuoka et al. (56) and support this grouping of all of these genes within the class B designation.

To help those in the field, GenBank numbers or references for sequences that have not been deposited are listed in Table 1. If a new gene sequence shows ≥80% amino acid homology to any member of a gene class and confers a similar phenotype to the host, we propose that the new gene be placed in the existing group and not be given a new letter or number designation. Thus, with classes that show a wide range of homologies, like class A (81% amino acid homology) or class O (84% amino acid homology), multiple members must be compared to the new gene. Note that the class designation is based on the amino acid sequence of the structural gene only and does not include the various regulatory sequences that can occur upstream of the gene. These guidelines are intended to apply to all of theN-methyltransferases, regardless of whether the gene was originally identified in pathogenic, opportunistic, normal flora bacteria or an antibiotic-producing species. Once all of the single capital letters have been used to identify new erm genes, we recommend naming genes as follows: erm(30),erm(31), etc. This system has been proposed for naming of new tet genes [tet(30), etc.] (52). Furthermore, a similar set of guidelines should be adopted for the genes that encode other mechanisms of resistance to any of the MLS antibiotics (Table 1). Class Y for gene erm(GM), class S for gene erm(SF), class T for geneerm(GT), class V for gene erm(SV), class X for genes erm(CD), erm(CX), and erm(A), and class 2 for gene srm(D) are new class designations that conform to the single-letter designation (Table 1).

There are a number of other methylase genes, most often found in methylase-producing organisms which have not been given ermdesignations, such as tlr(D), car(B),myr(B), and smr(A). All are from species which confer resistance to a 16-membered ring macrolide (Table 1). We have grouped and renamed them classes H for car(B), I formdm(A), N for tlr(D), O for genes lrmand srm(A), U for lmr(B), and W formyr(B). The clr gene could not be classified, because there is no sequence in the database or literature available. Less work has been done to determine if these genes are found outside their respective antibiotic producers (Table 3). erm genes are often linked with tet genes, and since genes conferring resistance to oxytetracycline, originally found in antibiotic-producing streptomycetes, are now found in some clinical Mycobacteriumisolates, it is certainly possible that some erm genes have also moved into Mycobacterium spp. and other genera (68).

To prevent two unrelated genes from being given the same designation, we propose to establish a reference center, as has recently been recommended for tetracycline resistance genes. By using the guideline presented above in governing the identification of new ermgenes, surveys can be conducted in bacterial populations to examine the spread of particular MLSB-resistant determinants. A single internal DNA fragment or oligonucleotide probe or a PCR assay that detects all members of a gene class can be established to screen large numbers of isolates. Not only will the adoption of a uniform naming system reduce the number of new erm gene names, but it will hopefully prevent confusion over unrelated genes being given the same designation and also prevent highly related genes from having different gene designations.

EFFLUX SYSTEMS

A number of different antibiotic resistance genes code for transport (efflux) proteins. These do not modify either the antibiotic or the antibiotic target, but instead pump the antibiotic out of the cell or the cellular membrane, keeping intracellular concentrations low and ribosomes free from antibiotic. Many of these proteins [mef(A), mef(E), andlmr(A)] have homology to the major facilitator superfamily (MFS) of efflux proteins. Others [car(A),msr(A), msr(B), ole(B),ole(C) srm(B), tlr(C), vga, and vga(B)] are putative members of the ABC transporter superfamily (70). In early years, most macrolide resistance was mediated by the presence of erm genes. However, more recently, other mechanisms of macrolide resistance have been found in increasing frequency in certain gram-positive populations (23, 27, 41, 43, 44, 92, 93, 106). Three different efflux systems which confer resistance have been described for gram-positive cocci [msr(A) (macrolide and streptogramin B resistant),mef(A) (macrolide efflux), and vga andvga(B) (virginiamycin factor A)] (4) (Table 2). Besides the academic interest in these genes, their presence in an erythromycin-resistant bacterial pathogen of interest may also have implications in terms of therapeutic choices. If an isolate carries amef gene, clindamycin can be considered, whereas the presence of an erm(B) gene would preclude consideration of a lincosamide. Recently, we and others have identifiedStreptococcus pneumoniae strains which carry bothmef and erm(B) genes and, as expected, have the MLSB phenotype (41, 53).

The mef genes have been found in a variety of gram-positive genera, including corynebacteria, enterococci, micrococci, and a variety of streptococcal species (30, 43, 53, 90) (Table3), suggesting a much wider distribution of this group of genes than originally imagined. Many of these genes are associated with conjugative elements located in the chromosome and are readily transferred conjugally across species and genus barriers (43, 53).

Two mef genes have been characterized in the literature:mef(A) (23) and mef(E) (94). The mef(A) gene was described inStreptococcus pyogenes, while the mef(E) gene was found in S. pneumoniae. Since the two genes share 90% DNA and 91% amino acid homology (Table 2), we recommended that these two genes be considered a single class, A: mef(A) gene and Mef(A) protein (Table 2).

The msr(A), msr(SA), msr(SA)′, andmsr(B) group differs from the mef genes because they confer resistance to both macrolide and streptogramin B antibiotics (MS) (13, 55-57). The msr(B) gene is roughly half the size of msr(A), but very homologous to it. Though this gene is significantly shorter than the msr(A) gene sequence, we placed it with the other msr genes (Table2).

In antibiotic producers, there are efflux pumps specific for MLSB antibiotics that generally belong to the ABC transporter superfamily (87). They include car(A) from Streptomyces thermotolerans (87),ole(B) from Streptomyces antibioticus (7, 80), srm(B) from Streptomyces ambofaciens(73), lmr(C) from Streptomyces lincolnensis (70), and tlr(C) fromStreptomyces fradiae (87). In addition to themsr(A) efflux pumps, there are two efflux systems identified in staphylococci that confer resistance to streptogramin A antibiotics,vga and vga(B) (4). Besidesmef(A), other efflux proteins that appear to be fueled by the proton motive force have been described for MLSBantibiotics. A lincomycin-specific efflux pump encoded bylmr(A) has been described in S. lincolnensis(110).

OTHER MECHANISMS

A variety of other mechanisms which usually confer resistance to only one of the three classes (M, L, or S) or one component such as streptogramin A, but not streptogramin B, have been described (103) (Table 2). These proteins modify the antibiotic rather than the rRNA target or serve as pumps that shuttle the antibiotic out of the bacterial cell. Enzymes which hydrolyze streptogramin B [vgb (virginiamycin factor B hydrolase), vgb(B) genes] or modify the antibiotic by adding an acetyl group (acetyltransferases) to streptogramin A [vat(virginiamycin, factor A acetylation), vat(B),vat(C), sat(A), and sat(G) genes] have been described (1-6) (Table 2). Many of these genes are plasmid borne, and often these vat-related genes [vat, vat(B), and vat(C) genes] are downstream of other genes encoding resistance to streptogramins [vgb, vga(B), and vgb(B) genes, respectively] in staphylococci (2), but not in enterococci (72). The acetyltransferase genes are related, in the active site region, to a novel chloramphenicol acetyltransferase family of enzymes. We have renamed sat(A) as vat(D) andsat(G) as vat(E) to simplify the nomenclature (Table 2).

Unlike most of the other genes described in this review, both theere (erythromycin esterification) and mph(macrolide phosphotransferase) genes (Table 2) were first described inE. coli rather than gram-positive cocci (8, 63, 64, 66, 67). According to our guidelines, mph(K) has been reassigned to mph(A), because there are only 10 amino acid (1%) differences between the two proteins. mph(BM) andmph(C) (66a) are grouped under Mph(C), because these genes are nearly identical to each other and distinct frommph(A) and mph(B) (Table 2). Several lincomycin nucleotidyltransferases have been identified: lin(A) inStaphylococcus haemolyticus (16),lin(A)′ in Staphylococcus aureus (17), and lin(B) in Enterococcus faecium(14). We propose changing lin(A) andlin(B) to lnu(A) and lnu(B) (for lincomycin nucleotidyltransferase), because the former letters have already been used for gamma BHC dehydrochlorinase and cyclohexadiene hydrolase genes. It is suggested that prior to naming a new gene class, it is necessary to determine if the proposed three-letter designation has been used for other previously characterized genes.

CONCLUSIONS

With the introduction of the newer, more stable macrolides with enhanced properties, there has been a significant increase in macrolide usage. Macrolides like azithromycin and clarithromycin are recommended for prophylactic use to prevent Mycobacterium avium complex disease in human immunodeficiency virus patients. As macrolide use increases, so does its exposure to bacterial populations, increasing the opportunity for bacteria to acquire macrolide or MLS resistance. Given that intragenic transfer of macrolide-resistant determinants is possible (15), it is likely that all of the genes described in this review will spread into new species and that new genes will be identified. Therefore, it is important to clarify the nomenclature of these resistance genes for their expanding audience.

ACKNOWLEDGMENTS

We thank M. Matsuoka for providing unpublished material; B. Weisblum for discussions; J. Davies, C. J. Smith, and S. Schwarz for reading the manuscript; and S. Lerner for doing sequence comparisons.

  • Copyright © 1999 American Society for Microbiology

REFERENCES

  1. 1.↵
    1. Allignet J.,
    2. El Solh N.
    Diversity among the gram-positive acetyltransferases inactivating streptogramin A and structurally related compounds and characterization of a new staphylococcal determinant, vatB. Antimicrob. Agents Chemother. 39 1995 2027 2036
    OpenUrlAbstract/FREE Full Text
  2. 2.↵
    1. Allignet J.,
    2. Liassine N.,
    3. El Solh N.
    Characterization of a staphylococcal plasmid related to pUB110 and carrying two novel genes, vatC and vgbB, encoding resistance to streptogramins A and B and similar antibiotics. Antimicrob. Agents Chemother. 42 1998 1794 1798
    OpenUrlAbstract/FREE Full Text
  3. 3.↵
    1. Allignet J.,
    2. Loncle V.,
    3. Simenel C.,
    4. Delepierre M.,
    5. El Solh N.
    Sequence of a staphylococcal gene, vat, encoding an acetyltransferase inactivating the A-type compounds of virginiamycin-like antibiotics. Gene 130 1993 91 98
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    1. Allignet J.,
    2. Loncle V.,
    3. El Solh N.
    Sequence of a staphylococcal plasmid gene, vga, encoding a putative ATP-binding protein involved in resistance to virginianmycin A-like antibiotics. Gene 117 1992 45 51
    OpenUrlCrossRefPubMedWeb of Science
  5. 5.↵
    1. Allignet J.,
    2. Loncle V.,
    3. Mazodier P.,
    4. El Solh N.
    Nucleotide sequence of a staphylococcal plasmid gene, vgb, encoding a hydrolase inactivating the B components of virginiamycin-like antibiotics. Plasmid 20 1988 271 275
    OpenUrlCrossRefPubMedWeb of Science
  6. 6.↵
    1. Allignet J.,
    2. El Solh N.
    Diversity among the gram-positive acetyltransferases inactivating streptogramin A and structurally related compounds and characterization of a new staphylococcal determinant, vatB. Antimicrob. Agents Chemother. 39 1995 2027 2036
    OpenUrlAbstract/FREE Full Text
  7. 7.↵
    1. Aparicio G.,
    2. Buche A.,
    3. Mendez C.,
    4. Salas J.-A.
    Characterization of the ATPase activity of the N-terminal nucleotide binding domain of an ABC transporter involved in oleandomycin secretion by Streptomyces antibioticus. FEMS Microbiol. Lett. 141 1996 157 162
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    1. Arthur M.,
    2. Andremont A.,
    3. Courvalin P.
    Distribution of erythromycin esterase and rRNA methylase genes in members of the family Enterobacteriaceae highly resistant to erythromycin. Antimicrob. Agents Chemother. 31 1987 404 409
    OpenUrlAbstract/FREE Full Text
  9. 9.↵
    1. Arthur M.,
    2. Brisson-Noel A.,
    3. Courvalin P.
    Origin and evolution of genes specifying resistance to macrolides, lincosamides and streptogramin antibiotics: data and hypothesis. J. Antimicrob. Chemother. 20 1987 783 802
    OpenUrlCrossRefPubMedWeb of Science
  10. 10.
    1. Berryman D. I.,
    2. Rood J. I.
    Cloning and hybridization analysis of ermP, a macrolide-lincosamide-streptogramin B resistance determinant from Clostridium perfringens. Antimicrob. Agents Chemother. 33 1989 1346 1353
    OpenUrlAbstract/FREE Full Text
  11. 11.
    1. Berryman D. I.,
    2. Rood J. I.
    The closely related ermB-ermAM genes from Clostridium perfringens,Enterococcus faecalis (pAMβ1), and Streptococcus agalactiae (pIP501) are flanked by variants of a directly repeated sequence. Antimicrob. Agents Chemother. 39 1995 1830 1834
    OpenUrlAbstract/FREE Full Text
  12. 12.
    1. Berryman D. I.,
    2. Lyristis M.,
    3. Rood J. I.
    Cloning and sequence analysis of ermQ, the predominant macrolide-lincosamide-streptogramin B resistance gene in Clostridium perfringens. Antimicrob. Agents Chemother. 38 1994 1041 1046
    OpenUrlAbstract/FREE Full Text
  13. 13.↵
    1. Beyer D.,
    2. Pepper K.
    The streptogramin antibiotics: update on their mechanism of action. Exp. Opin. Investig. Drugs 7 1998 591 599
    OpenUrl
  14. 14.↵
    1. Bozdogan B.,
    2. Berrezouga L.,
    3. Kuo M.-S.,
    4. Yurek D. A.,
    5. Farley K. A.,
    6. Stockman B. J.,
    7. LeClercq R.
    A new resistance gene, linB, conferring resistance to lincosamides by nucleotidylation in Enterococcus faecium HM1025. Antimicrob. Agents Chemother. 43 1999 925 929
    OpenUrlAbstract/FREE Full Text
  15. 15.↵
    1. Brisson-Noël A.,
    2. Arthur M.,
    3. Courvalin P.
    Evidence for natural gene transfer from gram-positive cocci to Escherichia coli. J. Bacteriol. 170 1988 1739 1745
    OpenUrlAbstract/FREE Full Text
  16. 16.↵
    1. Brisson-Noel A.,
    2. Courvalin P.
    Nucleotide sequence of gene linA encoding resistance to lincosamides in Staphylococcus haemolyticus. Gene 43 1986 247 253
    OpenUrlCrossRefPubMedWeb of Science
  17. 17.↵
    1. Brisson-Noel A.,
    2. Delrieu P.,
    3. Samain D.,
    4. Courvalin P.
    Inactivation of lincosaminide antibiotics in Staphylococcus. Identification of lincosaminide O-nucleotidyltransferases and comparison of the corresponding resistance genes. J. Biol. Chem. 263 1988 15880 15887
    OpenUrlAbstract/FREE Full Text
  18. 18.
    1. Calcutt M. J.,
    2. Cundliffe E.
    Cloning of a lincosamide resistance determinant from Streptomyces caelestis, the producer of celesticetin, and characterization of the resistance mechanism. J. Bacteriol. 172 1990 4710 4714
    OpenUrlAbstract/FREE Full Text
  19. 19.
    1. Cheng J.,
    2. Grebe T.,
    3. Wondrack L.,
    4. Courvalin P.,
    5. Sutcliffe J.
    Characterization of genes involved in erythromycin resistance in a clinical strain of Staphylococcus aureus, abstr. 837 Program and abstracts of the 39th Interscience Conference on Antimicrobial Agents and Chemotherapy. 1999 114 American Society for Microbiology Washington, D.C.
  20. 20.↵
    1. Choi S.-S.,
    2. Kim S.-K.,
    3. Oh T.-G.,
    4. Choi E.-C.
    Role of mRNA termination in regulation of ermK. J. Bacteriol. 179 1997 2065 2067
    OpenUrlAbstract/FREE Full Text
  21. 21.↵
    1. Chu D.
    Recent developments in 14- and 15-membered macrolides. Exp. Opin. Investig. Drugs 4 1995 65 94
    OpenUrl
  22. 22.
    1. Chung W. O.,
    2. Werckenthin C.,
    3. Schwarz S.,
    4. Roberts M. C.
    Host range of the ermF rRNA methylase gene in human and animal bacteria. J. Antimicrob. Chemother. 43 1999 5 14
    OpenUrlCrossRefPubMedWeb of Science
  23. 23.↵
    1. Clancy J.,
    2. Petitpas J. W.,
    3. Dib-Hajj F.,
    4. Yuan W.,
    5. Cronan M.,
    6. Kamath A.,
    7. Bergeron J.,
    8. Retsema J.
    Molecular cloning and functional analysis of a novel macrolide-resistance determinant mefA from Streptococcus pyogenes. Mol. Microbiol. 22 1996 867 879
    OpenUrlCrossRefPubMedWeb of Science
  24. 24.↵
    1. Clewell D. B.,
    2. Flannagan S. E.,
    3. Jaworski D. D.
    Unconstrained bacterial promiscuity: the Tn916-Tn1545 family of conjugative transposons. Trends Microbiol. 3 1995 229 236
    OpenUrlCrossRefPubMedWeb of Science
  25. 25.
    1. Cooper A. J.,
    2. Shoemaker N. B.,
    3. Salyers A. A.
    The erythromycin resistance gene from the Bacteroides conjugal transposon Tcr Emr 7853 is nearly identical to ermG from Bacillus sphaericus. Antimicrob. Agents Chemother. 40 1996 506 508
    OpenUrlAbstract/FREE Full Text
  26. 26.↵
    Council of Biology Editors, Inc CBE style manual: a guide for authors, editors, and publishers in the biological sciences 5th ed. 1983 Council of Biology, Editors, Inc. Bethesda, Md
  27. 27.↵
    1. Eady E. A.,
    2. Ross J. I.,
    3. Tipper J. L.,
    4. Walters C. E.,
    5. Cove J. H.,
    6. Noble W. C.
    Distribution of genes encoding erythromycin ribosomal methylases and an erythromycin efflux pump in epidemiologically distinct groups of staphylococci. J. Antimicrob. Chemother. 31 1993 211 217
    OpenUrlCrossRefPubMedWeb of Science
  28. 28.
    1. Epp J. K.,
    2. Burgett S. G.,
    3. Schoner G. E.
    Cloning and nucleotide sequence of a carbomycin-resistance gene from Streptomyces thermotolerans. Gene 53 1987 73 83
    OpenUrlCrossRefPubMedWeb of Science
  29. 29.
    Farrow, K. A., D. Lyras, and J. I. Rood. GenBank accession no. AF109075
  30. 30.↵
    1. Fraimow H.,
    2. Knob C.
    Amplification of macrolide efflux pumps msr and mef from Enterococcus faecium by polymerase chain reaction, abstr. A-125 Abstracts of the 98th General Meeting of the American Society for Microbiology. 1997 22 American Society for Microbiology Washington, D.C.
  31. 31.
    1. Hächler H.,
    2. Kayser F. H.,
    3. Berger-Bächi B.
    Homology of a transferable tetracycline resistance determinant of Clostridium difficile with Streptococcus (Enterococcus) faecalis transposon Tn916. Antimicrob. Agents Chemother. 31 1987 1033 1038
    OpenUrlAbstract/FREE Full Text
  32. 32.↵
    1. Halula M.,
    2. Manning S.,
    3. Macrina F. L.
    Nucleotide sequence of ermFU, macrolide-lincosamide-streptogramin (MLS) resistance gene encoding an RNA methylase from the conjugal element of Bacteroides fragilis V503. Nucleic Acids Res. 19 1991 3453
    OpenUrlCrossRefPubMedWeb of Science
  33. 33.
    1. Hammerum A. M.,
    2. Jensen L.,
    3. Bogo L.,
    4. Aarestrup F. M.
    Detection of the satA gene and transferability of virginiamycin resistance in Enterococcus faecium from food-animals. FEMS Microbiol. Lett. 168 1998 145 151
    OpenUrlCrossRefPubMedWeb of Science
  34. 34.
    1. Hara Q.,
    2. Hutchinson C. R.
    Cloning of midecamycin (MLS)-resistance genes from Streptomyces mycarofaciens,Streptomyces lividans and Streptomyces coelicolor A3(2). J. Antibiot. (Tokyo) 43 1990 977 991
    OpenUrlPubMed
  35. 35.
    1. Hodgson A. L. M.,
    2. Krywult J.,
    3. Radford A. J.
    Nucleotide sequence of the erythromycin resistance gene from Corynebacterium plasmid pNG2. Nucleic Acids Res. 18 1990 1891
    OpenUrlCrossRefPubMedWeb of Science
  36. 36.↵
    1. Hudson C. R.,
    2. Roberts M. C.,
    3. Gherardini F. C.
    Evidence of conjugal transfer of an erythromycin-resistance determinant in Borrelia burgdorferi, abstr. D-2 Abstracts of the 98th Annual Meeting of the American Society for Microbiology. 1998 223 American Society for Microbiology Washington, D.C.
  37. 37.
    1. Inouye M.,
    2. Morohoshi T.,
    3. Horinouchi S.,
    4. Beppu T.
    Cloning and sequences of two macrolides-resistance-encoding genes from mycinamicin-producing Micromonospora griseorubida. Gene 141 1994 39 46
    OpenUrlCrossRefPubMedWeb of Science
  38. 38.
    1. Jenkins G.,
    2. Zalacain M.,
    3. Cundliffe E.
    Inducible ribosomal RNA methylation in Streptomyces lividans, conferring resistance to lincomycin. J. Gen. Microbiol. 129 1989 2703 2714
    OpenUrl
  39. 39.
    1. Jensen L. B.,
    2. Hammerum A. M.,
    3. Aarestrup F. M.,
    4. van den Bogaard A. E.,
    5. Stobberingh E. E.
    Occurrence of satA and vgb genes in streptogramin-resistant Enterococcus faecium isolates of animal and human origins in The Netherlands. Antimicrob. Agents Chemother. 42 1998 3330 3331
    OpenUrlFREE Full Text
  40. 40.
    1. Jensen L. B.,
    2. Frimodt-Moller N.,
    3. Aarestrup F. M.
    Presence of erm gene classes in Gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiol. Lett. 170 1999 151 158
    OpenUrlCrossRefPubMedWeb of Science
  41. 41.↵
    1. Johnston N. J.,
    2. de Azavedo J. C.,
    3. Kellner J. D.,
    4. Low D. E.
    Prevalence and characterization of the mechanisms of macrolide, lincosamide, and streptogramin resistance in isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 42 1998 2425 2426
    OpenUrlAbstract/FREE Full Text
  42. 42.
    1. Kamimiya S.,
    2. Weisblum B.
    GenBank deposit: Streptomyces viridochromogenes rRNA (adenine-N6-) methyltransferase, ermSV gene. Accession no. U59450 1996
  43. 43.↵
    1. Kataja J.,
    2. Seppälä H.,
    3. Skurnik M.,
    4. Sarkkinen H.,
    5. Huovinen P.
    Different erythromycin resistance mechanisms in group C and group G streptococci. Antimicrob. Agents Chemother. 42 1998 1493 1494
    OpenUrlAbstract/FREE Full Text
  44. 44.↵
    1. Kataja J.,
    2. Huovinen P.,
    3. Skurnik M.,
    4. the Finnish Study Group for Antimicrobial Resistance,
    5. Seppälä H.
    Erythromycin resistance genes in group A streptococci in Finland. Antimicrob. Agents Chemother. 43 1999 48 52
    OpenUrlAbstract/FREE Full Text
  45. 45.
    1. Kim S.-K.,
    2. Baek M.-C.,
    3. Choi S.-S.,
    4. Kim B.-K.,
    5. Choi E.-C.
    Nucleotide sequence, expression and transcriptional analysis of the Escherichia coli mphK gene encoding macrolide-phosphotransferase K. Mol. Cells 6 1996 153 160
    OpenUrl
  46. 46.
    1. Kovalic D.,
    2. Giannattasio R. B.,
    3. Jin H.-J.,
    4. Weisblum B.
    23S rRNA domain V, a fragment that can be specifically methylated in vitro by the ErmSF (TlrA) methyltransferase. J. Bacteriol. 176 1994 6992 6998
    OpenUrlAbstract/FREE Full Text
  47. 47.↵
    1. Leclercq R.,
    2. Courvalin P.
    Bacterial resistance to macrolide, lincosamide, and streptogramin antibiotics by target modification. Antimicrob. Agents Chemother. 35 1991 1267 1272
    OpenUrlFREE Full Text
  48. 48.
    1. Leclercq R.,
    2. Courvalin P.
    Intrinsic and unusual resistance to macrolide, lincosamide, and streptogramin antibiotics in bacteria. Antimicrob. Agents Chemother. 35 1991 1273 1276
    OpenUrlFREE Full Text
  49. 49.
    1. Le Goffic F.,
    2. Capmau M. L.,
    3. Bonnet M. L.,
    4. Cerceau C.,
    5. Soussy C. J.,
    6. Dublanchet A.,
    7. Duval J.
    Plasmid-mediated pristinamycin resistance: PH1A, a pristinamycin 1A hydrolase. Ann. Inst. Pasteur 128 1977 471 474
    OpenUrl
  50. 50.
    1. Le Goffic F.,
    2. Capmau M. L.,
    3. Bonnet M. L.,
    4. Cerceau C.,
    5. Soussy C. J.,
    6. Dublanchet A.,
    7. Duval J.
    Plasmid-mediated pristinamycin resistance: PCIIA, a new enzyme which modifies pristinamycin IIA. J. Antibiot. 30 1977 665 669
    OpenUrlPubMed
  51. 51.↵
    1. Levy S. B.,
    2. McMurry L. M.,
    3. Burdett V.,
    4. Courvalin P.,
    5. Hillen W.,
    6. Roberts M. C.,
    7. Taylor D. E.
    Nomenclature for tetracycline resistance determinants. Antimicrob. Agents Chemother. 33 1989 1373 1374
    OpenUrlAbstract/FREE Full Text
  52. 52.↵
    1. Levy S. B.,
    2. McMurry L. M.,
    3. Barbosa T. M.,
    4. Burdett V.,
    5. Courvalin P.,
    6. Hillen W.,
    7. Roberts M. C.,
    8. Rood J. I.,
    9. Taylor D. E.
    Nomenclature for new tetracycline resistance determinants. Antimicrob. Agents Chemother. 43 1999 1523 1524
    OpenUrlAbstract/FREE Full Text
  53. 53.↵
    1. Luna V. A.,
    2. Coates P.,
    3. Eady E. A.,
    4. Cove J.,
    5. Nguyen T. T. H.,
    6. Roberts M. C.
    A variety of Gram-positive bacteria carry mobile mef genes. J. Antimicrob. Chemother. 44 1999 19 25
    OpenUrlCrossRefPubMedWeb of Science
  54. 54.
    1. Matsuoka M.,
    2. Inoue M.,
    3. Nakajima Y.
    A mechanism of resistance to partial macrolide and streptogramin B antibiotics in Staphylococcus aureus clinically isolated in Hungary. Biol. Pharm. Bull. 18 1995 1482 1486
    OpenUrlCrossRefPubMed
  55. 55.↵
    1. Matsuoka M.,
    2. Inoue M.,
    3. Nakajima Y.
    A dyadic plasmid that shows MLS and PMS resistance in Staphylococcus aureus. FEMS Microbiol. Lett. 148 1997 91 96
    OpenUrlCrossRefPubMedWeb of Science
  56. 56.↵
    1. Matsuoka M.,
    2. Inoue M.,
    3. Nakajima Y.
    A new class of erm genes mediating MLS-coresistance in Staphylococcus aureus: it resides on plasmid pMS97 together with msrSA′ gene coding for an active efflux pump, abstr. C-35 Abstracts of the 38th Interscience Conference on Antimicrobial Agents and Chemotherapy. 1998 78 American Society for Microbiology Washington, D.C.
  57. 57.↵
    1. Matsuoka M.,
    2. Endou K.,
    3. Kobayashi H.,
    4. Inoue M.,
    5. Nakajima Y.
    A plasmid that encodes three genes for resistance to macrolide antibiotics in Staphylococcus aureus. FEMS Microbiol. Lett. 167 1998 221 227
    OpenUrlCrossRefPubMedWeb of Science
  58. 58.↵
    1. Meier A.,
    2. Kirschner P.,
    3. Springer B.,
    4. Steingrube V. A.,
    5. Brown B. A.,
    6. Wallace R. J. Jr.,
    7. Böttger E. C.
    Identification of mutations in the 23S rRNA gene of clarithromycin-resistant Mycobacterium intracellulare. Antimicrob. Agents Chemother. 38 1994 381 384
    OpenUrlAbstract/FREE Full Text
  59. 59.
    1. Miller E. S.,
    2. Woese C. R.,
    3. Brenner S.
    Description of the erythromycin-producing bacterium Arthrobacter sp. strain NRRL B-3381 as Aeromicrobium erythreum gen. nov., sp. nov. Int. J. Syst. Bacteriol. 41 1991 363 368
    OpenUrlCrossRefPubMed
  60. 60.
    1. Milton I. D.,
    2. Hewitt C. L.,
    3. Harwood C. R.
    Cloning and sequencing of a plasmid-mediated erythromycin resistance determinant from Staphylococcus xylosus. FEMS Microbiol. Lett. 76 1992 141 147
    OpenUrlPubMed
  61. 61.
    1. Monod M.,
    2. Denoya C.,
    3. Dubnau D.
    Sequence and properties of pIM13, a macrolide-lincosamide-streptogramin B resistance plasmid from Bacillus subtilis. J. Bacteriol. 167 1986 138 147
    OpenUrlAbstract/FREE Full Text
  62. 62.
    1. Monod M.,
    2. Mohan S.,
    3. Dubnau D.
    Cloning and analysis of ermG, a new macrolide-lincosamide-streptogramin B resistance element from Bacillus sphaericus. J. Bacteriol. 169 1987 340 350
    OpenUrlAbstract/FREE Full Text
  63. 63.↵
    1. Noguchi N.,
    2. Emura A.,
    3. Matsuyama H.,
    4. O’Hara K.,
    5. Sasatsu M.,
    6. Kono M.
    Nucleotide sequence and characterization of erythromycin resistance determinant that encodes macrolide 2′-phosphotransferase I in Escherichia coli. Antimicrob. Agents Chemother. 39 1995 2359 2363
    OpenUrlAbstract/FREE Full Text
  64. 64.↵
    1. Noguchi N.,
    2. Katayama J.,
    3. O’Hara K.
    Cloning and nucleotide sequence of the mphB gene for macrolide 2′-phosphotransferase II in Escherichia coli. FEMS Microbiol. Lett. 144 1996 197 202
    OpenUrlCrossRefPubMedWeb of Science
  65. 65.
    1. Oh T.-G.,
    2. Kwon A.-R.,
    3. Choi E.-C.
    Induction of ermAMR from a clinical strain of Enterococcus faecalis by 16-membered-ring macrolide antibiotics. J. Bacteriol. 180 1998 5788 5791
    OpenUrlAbstract/FREE Full Text
  66. 66.↵
    1. O’Hara K.,
    2. Kanda T.,
    3. Ohmiya K.,
    4. Ebisu T.,
    5. Kono M.
    Purification and characterization of macrolide 2′-phosphotransferase from a strain of Escherichia coli that is highly resistant to erythromycin. Antimicrob. Agents Chemother. 33 1989 1354 1357
    OpenUrlAbstract/FREE Full Text
  67. 66a.↵
    O’Hara, K. Personal communication.
  68. 67.↵
    1. Ounissi H.,
    2. Courvalin P.
    Nucleotide sequence of the gene ereA encoding the erythromycin esterase in Escherichia coli. Gene 35 1985 271 278
    OpenUrlCrossRefPubMedWeb of Science
  69. 68.↵
    1. Pang Y.,
    2. Brown B. A.,
    3. Steingrube V. A.,
    4. Wallace R. J. Jr.,
    5. Roberts M. C.
    Tetracycline resistance determinants in Mycobacterium and Streptomyces species. Antimicrob. Agents Chemother. 38 1994 1408 1412
    OpenUrlAbstract/FREE Full Text
  70. 69.
    1. Pernodet J. L.,
    2. Blondelet-Rouault M. H.,
    3. Guerineau M.
    Resistance to spiramycin in Streptomyces ambofaciens, the producer organism, involves at least two different mechanisms. J. Gen. Microbiol. 139 1993 1003 1011
    OpenUrlCrossRefPubMed
  71. 70.↵
    1. Peschke U.,
    2. Schmidt H.,
    3. Zhang H.-Z.,
    4. Piepersberg W.
    Molecular characterization of the lincomycin-production gene cluster of Streptomyces lincolnensis 78-11. Mol. Microbiol. 16 1995 1137 1156
    OpenUrlCrossRefPubMedWeb of Science
  72. 71.↵
    1. Rasmussen J. L.,
    2. Odelson D. A.,
    3. Macrina F. L.
    Complete nucleotide sequence and transcription of ermF, a macrolide-lincosamide-streptogramin B resistance determinant from Bacteroides fragilis. J. Bacteriol. 168 1986 523 533
    OpenUrlAbstract/FREE Full Text
  73. 72.↵
    1. Rende-Fournier R.,
    2. LeClercq R.,
    3. Galimand M.,
    4. Duval J.,
    5. Courvalin P.
    Identification of the satA gene encoding a streptogramin A acetyltransferase in Enterococcus faecium BM4145. Antimicrob. Agents Chemother. 37 1993 2119 2125
    OpenUrlAbstract/FREE Full Text
  74. 73.↵
    1. Richardson M. A.,
    2. Kuhstoss S.,
    3. Solenberg P.,
    4. Schaus N. A.,
    5. Rao R. N.
    A new shuttle cosmid vector, pKC505, for streptomycetes: its use in the cloning of three different spiramycin-resistance genes from a Streptomyces ambovaciens library. Gene 61 1987 231 241
    OpenUrlCrossRefPubMedWeb of Science
  75. 74.
    1. Roberts A. N.,
    2. Hudson G. S.,
    3. Brenner S.
    An erythromycin-resistance gene from an erythromycin-producing strain of Arthrobacter sp. Gene 35 1985 259 270
    OpenUrlCrossRefPubMedWeb of Science
  76. 75.
    1. Roberts M. C.
    Distribution of tetracycline and macrolides-lincosamides-streptogramin B (MLS) genes in anaerobic bacteria. Clin. Infect. Dis. 20 1995 S367 S369
    OpenUrlCrossRefPubMed
  77. 76.↵
    1. Roberts M. C.,
    2. Brown M. B.
    Macrolide-lincosamide resistance determinants in streptococcal species isolated from the bovine mammary gland. Vet. Microbiol. 40 1994 253 261
    OpenUrlCrossRefPubMedWeb of Science
  78. 77.↵
    1. Roberts M. C.,
    2. Chung W. O.,
    3. Roe D. E.
    Characterization of tetracycline and erythromycin determinants in Treponema denticola. Antimicrob. Agents Chemother. 40 1996 1690 1694
    OpenUrlAbstract/FREE Full Text
  79. 78.↵
    1. Roberts M. C.,
    2. Chung W. O.,
    3. Roe D.,
    4. Xia M.,
    5. Marquez C.,
    6. Borthagaray G.,
    7. Whittington W. L.,
    8. Holmes K. K.
    Erythromycin-resistant Neisseria gonorrhoeae and oral commensal Neisseria spp. carry known rRNA methylase genes. Antimicrob. Agents Chemother. 43 1999 1367 1372
    OpenUrlAbstract/FREE Full Text
  80. 79.
    1. Roberts M. C.,
    2. McFarland L. V.,
    3. Mullany P.,
    4. Mulligan M. E.
    Characterization of the genetic basis of antibiotic resistance in Clostridium difficile. J. Antimicrob. Chemother. 33 1994 419 429
    OpenUrlCrossRefPubMedWeb of Science
  81. 80.↵
    1. Rodriguez A. M.,
    2. Olano C.,
    3. Vilches C.,
    4. Mendez C.,
    5. Salas J. A.
    Streptomyces antibioticus contains at least three olendomycin resistance determinants, one of which shows homology with proteins of the ABC-transporter superfamily. Mol. Microbiol. 8 1993 571 582
    OpenUrlCrossRefPubMed
  82. 81.
    1. Roe D. E.,
    2. Weinberg A.,
    3. Roberts M. C.
    Mobility of rRNA methylase genes in Campylobacter (Wolinella) rectus. J. Antimicrob. Chemother. 36 1995 738 740
    OpenUrlCrossRefPubMed
  83. 82.
    1. Roe D. E.,
    2. Weinberg A.,
    3. Roberts M. C.
    Mobile rRNA methylase genes in Actinobacillus actinomycetemcomitans. J. Antimicrob. Chemother. 37 1996 457 464
    OpenUrlCrossRefPubMedWeb of Science
  84. 83.
    1. Ross J. I.,
    2. Eady E. A.,
    3. Cove J. H.,
    4. Baumberg S.
    Minimal functional system required for expression of erythromycin resistance by msrA in Staphylococcus aureus RN4220. Gene 183 1996 143 148
    OpenUrlCrossRefPubMedWeb of Science
  85. 84.↵
    1. Ross J. I.,
    2. Eady E. A.,
    3. Cove J. H.,
    4. Jones C. E.,
    5. Ratyal A. H.,
    6. Miller Y. W.,
    7. Vyakrnam S.,
    8. Cunliffe W. J.
    Clinical resistance to erythromycin and clinidamycin in cutaneous propionibacteria isolated from acne patients is associated with mutations in 23S rRNA. Antimicrob. Agents Chemother. 41 1989 1162 1165
    OpenUrlAbstract/FREE Full Text
  86. 85.
    1. Rosteck P. R. Jr.,
    2. Reynolds P. A.,
    3. Hershberger C. L.
    Homology between proteins controlling Streptomyces fradiae tylosin resistance and ATP-binding transport. Gene 102 1991 27 32
    OpenUrlCrossRefPubMedWeb of Science
  87. 86.↵
    1. Salyers A. A.,
    2. Shoemaker N. B.,
    3. Stevens A. M.,
    4. Li L.-Y.
    Conjugative transposons: an unusual and diverse set of integrated gene transfer elements. Microbiol. Rev. 59 1995 579 590
    OpenUrlAbstract/FREE Full Text
  88. 87.↵
    1. Schoner B.,
    2. Geistlich M.,
    3. Rosteck P. I. Jr.,
    4. Rao R. N.,
    5. Seno E.,
    6. Reynolds P.,
    7. Cox K.,
    8. Burgett S.,
    9. Hershberger C.
    Sequence similarity between macrolide-resistance determinants and ATP-binding transport proteins. Gene 115 1992 93 96
    OpenUrlCrossRefPubMedWeb of Science
  89. 88.↵
    1. Seppälä H.,
    2. Skurnik M.,
    3. Soini H.,
    4. Roberts M. C.,
    5. Huovinen P.
    A novel erythromycin resistance methylase gene (ermTR) in Streptococcus pyogenes. Antimicrob. Agents Chemother. 42 1998 257 262
    OpenUrlAbstract/FREE Full Text
  90. 89.
    1. Shoemaker N. B.,
    2. Barber R. D.,
    3. Salyers A. A.
    Cloning and characterization of a Bacteroides conjugal tetracycline-erythromycin resistance element by using a shuttle cosmid vector. J. Bacteriol. 171 1989 1294 1302
    OpenUrlAbstract/FREE Full Text
  91. 90.↵
    1. Shortridge V. D.,
    2. Flamm R. K.,
    3. Ramer N.,
    4. Beyer J.,
    5. Tanaka S. K.
    Novel mechanism of macrolide resistance in Streptococcus pneumoniae. Diagn. Microbiol. Infect. Dis. 26 1996 73 78
    OpenUrlCrossRefPubMedWeb of Science
  92. 91.↵
    1. Smith C. J.
    Nucleotide sequence analysis of Tn4551: use of ermFS operon fusions to detect promoter activity in Bacteroides fragilis. J. Bacteriol. 169 1987 4589 4596
    OpenUrlAbstract/FREE Full Text
  93. 92.↵
    1. Sutcliffe J.,
    2. Grebe T.,
    3. Tait-Kamradt A.,
    4. Wondrack L.
    Detection of erythromycin-resistant determinants by PCR. Antimicrob. Agents Chemother. 40 1996 2562 2566
    OpenUrlAbstract/FREE Full Text
  94. 93.↵
    1. Sutcliffe J.,
    2. Tait-Kamradt A.,
    3. Wondrack L.
    Streptococcus pneumoniae and Streptococcus pyogenes resistant to macrolides but sensitive to clindamycin: a common resistance pattern mediated by an efflux system. Antimicrob. Agents Chemother. 40 1996 1817 1824
    OpenUrlAbstract/FREE Full Text
  95. 94.↵
    1. Tait-Kamradt A.,
    2. Clancy J.,
    3. Cronan M.,
    4. Dib-Hajj F.,
    5. Wondrack L.,
    6. Yuan W.,
    7. Sutcliffe J.
    mefE is necessary for the erythromycin-resistant M phenotype in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 41 1997 2251 2255
    OpenUrlAbstract/FREE Full Text
  96. 95.↵
    1. Trieu-Cuot P.,
    2. Poyart-Salmeron C.,
    3. Carlier C.,
    4. Courvalin P.
    Nucleotide sequence of the erythromycin resistance gene of the conjugative transposon Tn1545. Nucleic Acids Res. 18 1990 3660
    OpenUrlCrossRefPubMedWeb of Science
  97. 96.↵
    1. Vergis E. N.,
    2. Yu V. L.
    Macrolides are ideal for empiric therapy of community-acquired pneumonia in the immunocompetent host. Semin. Respir. Infect. 12 1997 322 328
    OpenUrlPubMed
  98. 97.↵
    1. Vergis E. N.,
    2. Yu V. L.
    New macrolides or new quinolones as monotherapy for patients with community-acquired pneumonia; our cup runneth over? Chest 113 1998 1158 1159
    OpenUrlCrossRefPubMedWeb of Science
  99. 98.
    1. Wasteson Y.,
    2. Robe D. E.,
    3. Falk K.,
    4. Roberts M. C.
    Characterization of tetracycline and erythromycin resistance in Actinobacillus pleuropneumoniae. Vet. Microbiol. 48 1996 41 50
    OpenUrlCrossRefPubMed
  100. 99.
    1. Weber J. M.,
    2. Leung J. O.,
    3. Main G. T.,
    4. Potenz R. H. B.,
    5. Paulus T. J.,
    6. DeWitt J. P.
    Organization of a cluster of erythromycin genes in Saccharopolyspora erythraea. J. Bacteriol. 172 1990 2372 2383
    OpenUrlAbstract/FREE Full Text
  101. 100.↵
    1. Weisblum B.
    Resistance to macrolide-lincosamide-streptogramin antibiotics Gram-positive pathogens. Fischetti V. A. 1999 682 698 American Society for Microbiology Washington, D.C.
  102. 101.↵
    1. Weisblum B.
    Erythromycin resistance by ribosome modification. Antimicrob. Agents Chemother. 39 1995 577 585
    OpenUrlFREE Full Text
  103. 102.↵
    1. Weisblum B.
    Insights into erythromycin action from studies of its activity as inducer of resistance. Antimicrob. Agents Chemother. 39 1995 797 805
    OpenUrlFREE Full Text
  104. 103.↵
    1. Weisblum B.
    Macrolide resistance. Drug Resist. Update 1 1998 29 41
    OpenUrlCrossRefPubMed
  105. 104.↵
    1. Werckenthin C.,
    2. Schwarz S.,
    3. Westh H.
    Structural alterations in the translational attenuator of constitutively expressed ermC genes. Antimicrob. Agents Chemother. 43 1999 1681 1685
    OpenUrlAbstract/FREE Full Text
  106. 105.
    1. Werner G.,
    2. Witte W.
    Characterization of a new enterococcal gene, satG, encoding a putative acetyltransferase conferring resistance to streptogramin A compounds. Antimicrob. Agents Chemother. 43 1999 1813 1814
    OpenUrlFREE Full Text
  107. 106.↵
    1. Widdowson C. A.,
    2. Klugman K. P.
    Emergence of the M phenotype of erythromycin-resistant pneumococci in South Africa. Emerg. Infect. Dis. 4 1998 277 281
    OpenUrlPubMedWeb of Science
  108. 107.↵
    1. Young H.,
    2. Moyes A.,
    3. McMillan A.
    Azithromycin and erythromycin resistant Neisseria gonorrhoeae following treatment with azithromycin. Int. J. Sex. Transm. Dis. AIDS 8 1997 299 302
    OpenUrl
  109. 108.
    1. Zalacain M.,
    2. Cundliffe E.
    Methylation of 23S rRNA caused by tlrA (ermSF), a tylosin resistance determinant from Streptomyces fradiae. J. Bacteriol. 171 1989 4254 4260
    OpenUrlAbstract/FREE Full Text
  110. 109.
    1. Zalacain M.,
    2. Cundliffe E.
    Cloning of tlrD, a fourth resistance gene, from the tylosin producer, Streptomyces fradiae. Gene 97 1991 137 142
    OpenUrlCrossRefPubMedWeb of Science
  111. 110.↵
    1. Zhang H.-Z.,
    2. Schmidt H.,
    3. Piepersberg W.
    Molecular cloning and characterization of two lincomycin-resistance genes, lmrA and lmrB, from Streptomyces lincolnensis 78-11. Mol. Microbiol. 6 1992 2147 2157
    OpenUrlCrossRefPubMed
PreviousNext
Back to top
Download PDF
Citation Tools
Nomenclature for Macrolide and Macrolide-Lincosamide-Streptogramin B Resistance Determinants
Marilyn C. Roberts, Joyce Sutcliffe, Patrice Courvalin, Lars Bogo Jensen, Julian Rood, Helena Seppala
Antimicrobial Agents and Chemotherapy Dec 1999, 43 (12) 2823-2830; DOI: 10.1128/AAC.43.12.2823

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Antimicrobial Agents and Chemotherapy article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Nomenclature for Macrolide and Macrolide-Lincosamide-Streptogramin B Resistance Determinants
(Your Name) has forwarded a page to you from Antimicrobial Agents and Chemotherapy
(Your Name) thought you would be interested in this article in Antimicrobial Agents and Chemotherapy.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Nomenclature for Macrolide and Macrolide-Lincosamide-Streptogramin B Resistance Determinants
Marilyn C. Roberts, Joyce Sutcliffe, Patrice Courvalin, Lars Bogo Jensen, Julian Rood, Helena Seppala
Antimicrobial Agents and Chemotherapy Dec 1999, 43 (12) 2823-2830; DOI: 10.1128/AAC.43.12.2823
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • RRNA METHYLASES
    • EFFLUX SYSTEMS
    • OTHER MECHANISMS
    • CONCLUSIONS
    • ACKNOWLEDGMENTS
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

Anti-Bacterial Agents
Drug Resistance, Microbial
Genes, Bacterial
macrolides
Terminology as Topic
Virginiamycin

Related Articles

Cited By...

About

  • About AAC
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • AAC Podcast
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #AACJournal

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Print ISSN: 0066-4804; Online ISSN: 1098-6596