The DOI matches its Crossref record; 242 of the 242 references it cites were found in a registry or an index.
Clinically Relevant Chromosomally Encoded Multidrug Resistance Efflux Pumps in Bacteria
Open accessAbstract
SUMMARY: Efflux pump genes and proteins are present in both antibiotic-susceptible and antibiotic-resistant bacteria. Pumps may be specific for one substrate or may transport a range of structurally dissimilar compounds (including antibiotics of multiple classes); such pumps can be associated with multiple drug (antibiotic) resistance (MDR). However, the clinical relevance of efflux-mediated resistance is species, drug, and infection dependent. This review focuses on chromosomally encoded pumps in bacteria that cause infections in humans. Recent structural data provide valuable insights into the mechanisms of drug transport. MDR efflux pumps contribute to antibiotic resistance in bacteria in several ways: (i) inherent resistance to an entire class of agents, (ii) inherent resistance to specific agents, and (iii) resistance conferred by overexpression of an efflux pump. Enhanced efflux can be mediated by mutations in (i) the local repressor gene, (ii) a global regulatory gene, (iii) the promoter region of the transporter gene, or (iv) insertion elements upstream of the transporter gene. Some data suggest that resistance nodulation division systems are important in pathogenicity and/or survival in a particular ecological niche. Inhibitors of various efflux pump systems have been described; typically these are plant alkaloids, but as yet no product has been marketed.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“There are 5 major families of efflux pumps, including i) the major facilitator superfamily (MFS), ii) the small multidrug resistance family (SMR), iii) the resistance-nodulation-cell-division family (RND), iv) the ATP-binding cassette family (ABC), and v) the multidrug and toxic compound extrusion family (MATE).”
From Mechanisms of Antibiotic Resistance (2016) · cites this paper as [46]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Items 201–242 of 242
Huda, M. N., Chen, J., Morita, Y., Kuroda, T., Mizushima, T., & Tsuchiya, T. (2003) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2003.tb03379.x · Cited by 61
Gerken, H. G., & Misra, R. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04301.x · Cited by 60
Evidence for Multiple-Antibiotic Resistance in Campylobacter jejuni Not Mediated by CmeB or CmeF
Pumbwe, L., Randall, L. P., Woodward, M. J., & Piddock, L. J. V. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.4.1289-1293.2005 · Cited by 59
Self-citationDefining a rob Regulon in Escherichia coli by Using Transposon Mutagenesis
Bennik, M. H. J., Pomposiello, P. J., Thorne, D. F., & Demple, B. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.13.3794-3801.2000 · Cited by 59
Cloning, Sequencing, and Characterization of the SdeAB Multidrug Efflux Pump of Serratia marcescens
Kumar, A., & Worobec, E. A. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.4.1495-1501.2005 · Cited by 58
Two Efflux Systems Expressed Simultaneously in Multidrug-Resistant Pseudomonas aeruginosa
Pumbwe, L., & Piddock, L. J. V. (2000) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.44.10.2861-2864.2000 · Cited by 58
Self-citationBoutoille, D., Corvec, S., Caroff, N., Giraudeau, C., Espaze, E., Caillon, J., Plésiat, P., & Reynaud, A. (2003) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(03)00882-6 · Cited by 57
Accumulation of 10 Fluoroquinolones by Wild-Type or Efflux Mutant Streptococcus pneumoniae
Piddock, L. J. V., & Johnson, M. M. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.3.813-820.2002 · Cited by 55
Self-citationBroskey, J. P. (2000) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/45.suppl_3.95 · Cited by 54
Shiba, T., Ishiguro, K., 竹本, 法., Koibuchi, H., & Sugimoto, K. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.20.5872-5877.1995 · Cited by 53
Aono, R., Kobayashi, M., Nakajima, H., & Kobayashi, H. (1995) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.59.213 · Cited by 51
Folster, J. P., & Shafer, W. M. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.11.3713-3720.2005 · Cited by 51
A pleiotropic, posttherapy, enoxacin-resistant mutant of Pseudomonas aeruginosa
Piddock, L. J. V., Hall, M. C., Bellido, F., Bains, M., & Hancock, R. E. W. (1992) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.36.5.1057 · Cited by 50
Self-citationXu, X., Xianzhong, S., Morita, Y., Kuroda, T., Mizushima, T., & Tsuchiya, T. (2003) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2003.tb03467.x · Cited by 49
Marrer, E., Satoh, A. T., Johnson, M. M., Piddock, L. J. V., & Page, M. G. P. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.50.1.269-278.2006 · Cited by 49
Self-citationBanerjee, S. K., Bhatt, K., Misra, P., & Chakraborti, P. K. (2000) · Molecular and General Genetics MGG · doi:10.1007/pl00008663 · Cited by 48
Noguchi, N., OKADA, H. M., Narui, K., & Sasatsu, M. (2004) · Microbial Drug Resistance · doi:10.1089/mdr.2004.10.197 · Cited by 48
Jones, M. E., Boenink, N. M., Verhoef, J., Köhrer, K., & Schmitz, F. (2000) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/45.3.353 · Cited by 48
Inhibitors of multidrug resistance (MDR) have affinity for MDR substrates
Zloh, M., Kaatz, G. W., & Gibbons, S. (2004) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2003.12.015 · Cited by 47
Braibant, M., Guilloteau, L. L. A., & Zygmunt, M. S. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.9.3050-3053.2002 · Cited by 45
Salmonella Gene rma ( ramA ) and Multiple-Drug-Resistant Salmonella enterica Serovar Typhimurium
van der Straaten, T., Janssen, R., Mevius, D. J., & van Dissel, J. T. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.6.2292-2294.2004 · Cited by 45
Dupont, P., Hocquet, D., Jeannot, K., Chavanet, P., & Plésiat, P. (2005) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dki030 · Cited by 44
Noguchi, N., Okihara, T., Namiki, Y., Kumaki, Y., Yamanaka, Y., Koyama, M., Wakasugi, K. O., & Sasatsu, M. (2005) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2004.11.016 · Cited by 41
Crystallographic analysis of AcrB
Pos, K. M., Schiefner, A., Seeger, M. A., & Diederichs, K. (2004) · FEBS Letters · doi:10.1016/s0014-5793(04)00272-8 · Cited by 41
Ordway, D. J., Hohmann, J., Viveiros, M., Viveiros, A., Molnar, J. A., Leandro, C., Arroz, M. J., Grácio, M. A. A., & Amaral, L. (2003) · Phytotherapy Research · doi:10.1002/ptr.1314 · Cited by 40
Chuanchuen, R., Gaynor, J. B., Karkhoff-Schweizer, R. R., & Schweizer, H. P. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.5.1844-1851.2005 · Cited by 36
Payne, D. N., Babb, J. R., & Bradley, C. R. (1999) · Letters in Applied Microbiology · doi:10.1046/j.1365-2672.1999.00482.x · Cited by 35
PDF Inhibitors: An Emerging Class of Antibacterial Drugs
Johnson, K., Lofland, D., & Moser, H. E. (2005) · Current Drug Targets - Infectious Disorders · doi:10.2174/1568005053174618 · Cited by 33
Schmitz, F., Hertel, B., Hofmann, B., Scheuring, S., Verhoef, J., Fluit, A. C., Heinz, H., Köhrer, K., & Jones, M. E. (1998) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/42.4.561 · Cited by 31
Cross, L. J. (2000) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/45.1.95 · Cited by 31
Cagliero, C. (2006) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkl212 · Cited by 30
Oizumi, N., Kawabata, S., Hirao, M., Watanabe, K., Okuno, S., Fujiwara, T., & Kikuchi, M. (2001) · Journal of Infection and Chemotherapy · doi:10.1007/s101560100034 · Cited by 28
Sequence similarity between multidrug resistance efflux pumps of the ABC and RND superfamilies
Kim, S. H., Chang, A. B., & Saier, M. H. (2004) · Microbiology · doi:10.1099/mic.0.27312-0 · Cited by 28
Livermore, D. M., & Davy, K. W. M. (1991) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.35.5.916 · Cited by 24
Pumbwe, L., Everett, M. J., Hancock, R. E. W., & Piddock, L. J. V. (1996) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1996.tb08456.x · Cited by 23
Self-citationSánchez, P. (2003) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkg181 · Cited by 23
Escribano, I., Rodrı́guez, J. C., Cebrián, L., & Royo, G. (2004) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2004.05.004 · Cited by 20
Contribution of Efflux to Cefuroxime Resistance in Clinical Isolates of Escherichia coli
Källman, O., Fendukly, F., Karlsson, I., & Kronvall, G. (2003) · Scandinavian Journal of Infectious Diseases · doi:10.1080/00365540310014639 · Cited by 15
Treatment of staphylococcal infection
Amyes, S. G. B. (2005) · BMJ · doi:10.1136/bmj.330.7498.976 · Cited by 11
Kurai, S., Urabe, H., & Ogawara, H. (1995) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.39.1.260 · Cited by 8
Cagliero, C., Cloix, L., Payot, S., & Cloeckaert, A. (2004) · HAL · Cited by 1
High-Level Fluoroquinolone-Resistant Clinical Isolates of Overproduce Multidrug Efflux Protein AcrA.
Mazzariol, A., Tokue, Y., Kanegawa, T., Cornaglia, G., & Nikaido, H. (2001) · Antimicrobial Agents and Chemotherapy · Cited by 1
Flagged first, then by citations
Research works printed but not linked: 2
- Alekshun, M. A., and S. B. Levy. 2004. The Escherichia coli mar locus—antibiotic resistance and more. ASM News70:451-456.
- Olliver, A., M. Valle, E. Chaslus-Dancla, and A. Cloeckaert. 2004. Role of an acrR mutation in multidrug resistance of in vitro selected fluoroquinolone-resistant mutants of Salmonella enterica serovar Typhimurium. FEMS Microbiol. Lett.238:267-272.
Cited by
Sorted by citations
Origins and evolution of antibiotic resistance
Davies, J., & Davies, D. (2010) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00016-10 · Cited by 5,784
Molecular mechanisms of antibiotic resistance
Blair, J. M. A., Webber, M. A., Baylay, A. J., Ogbolu, D. O., & Piddock, L. J. V. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3380 · Cited by 4,092
Self-citationAcinetobacter baumannii : Emergence of a Successful Pathogen
Peleg, A. Y., Seifert, H., & Paterson, D. L. (2008) · Clinical Microbiology Reviews · doi:10.1128/cmr.00058-07 · Cited by 3,416
Mechanisms of Antibiotic Resistance
Munita, J. M., & Arias, C. A. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.vmbf-0016-2015 · Cited by 2,782
An overview of the antimicrobial resistance mechanisms of bacteria
Reygaert, W. C. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.3.482 · Cited by 2,152
Metadata
- Authors
- Piddock, L. J. V.
- Affiliations
- University of Birmingham (GB)
- Corresponding author
- Piddock, Laura J. V.
- ORCID
- Piddock, Laura J. V.
- Venue
- Clinical Microbiology Reviews
- Publisher
- American Society for Microbiology
- Published
- 2006-04
- Volume
- 19
- Issue
- 2
- Pages
- 382-402
- ISSN
- 0893-8512 (ISSN-L)
- 1098-6618
- PMC
- PMC1471989
- OpenAlex
- W2112586763
- Cited by
- 1,231
- References
- 242
- Citations by year
- 2026: 37 · 2025: 45 · 2024: 66 · 2023: 65 · 2022: 69 · 2021: 99 · 2020: 75 · 2019: 69 · 2018: 53 · 2017: 79 · 2016: 72 · 2015: 69 · 2014: 72 · 2013: 57 · 2012: 63
- FWCI
- 2.45
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Clinical Microbiology Reviews (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Topics
- Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- multidrug resistance, efflux pumps, antibiotic resistance, pathogenic bacteria, efflux pump regulation, efflux pump inhibitors, plant alkaloids, drug transport mechanisms, insertion elements
- MeSH terms
- Alkaloids, Anti-Infective Agents, Bacteria, Bacterial Proteins, Biological Transport, Chromosomes, Bacterial, Disinfectants, DNA Transposable Elements, Genes, Regulator, Mutation, Promoter Regions, Genetic, Virulence, Drug Resistance, Multiple, Bacterial, Membrane Transport Proteins, ATP-Binding Cassette, Sub-Family C Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
