Research progress in a novel mobile RND efflux pump TMexCD-TOprJ
Author:
  • Article
  • | |
  • Metrics
  • |
  • Reference [75]
  • |
  • Related [20]
  • | | |
  • Comments
    Abstract:

    Antibiotics are considered one of the cornerstones of modern medicine. However, the abuse of antimicrobial agents, including antibiotics, has accelerated the emergence of super bacteria that can resist multiple antimicrobial agents. Resistance genes are the key factors leading to bacterial resistance and can be horizontally transmitted by mobile genetic elements (MGEs), such as plasmids, transposons, and insertion sequences, posing a serious threat to public health. In recent years, facing the outbreak of carbapenem-resistant and polymyxin-resistant bacteria, tigecycline has been regarded as the “last line of defense” against multiple drug-resistant bacterial infections in humans. Recently, a novel mobile efflux pump gene cluster tmexCD-toprJ, mainly existing in plasmids, was found. This gene cluster encodes resistance-nodulation-cell division (RND) efflux pumps, which can expel a variety of antibiotics, including tigecycline, out of bacteria, greatly enhancing the resistance of bacteria. The tmexCD-toprJ gene cluster has been horizontally transferred to humans, animals, and the environment by mobile elements such as plasmids, posing a serious threat to public health. However, research on the specific structure and functional mechanism of TMexCD-TOprJ remains to be carried out. This article systematically summarizes the distribution characteristics, transmission mechanisms, and efflux pump structures of tmexCD-toprJ and proposes measures to block its spread from the concept of One Health, offering a scientific basis for slowing down the dissemination of tmexCD-toprJ.

    Reference
    [1] ROSSOLINI GM, ARENA F, PECILE P, POLLINI S. Update on the antibiotic resistance crisis[J]. Current Opinion in Pharmacology, 2014, 18: 56-60.
    [2] FERRI M, RANUCCI E, ROMAGNOLI P, GIACCONE V. Antimicrobial resistance: a global emerging threat to public health systems[J]. Critical Reviews in Food Science and Nutrition, 2017, 57(13): 2857-2876.
    [3] PIDDOCK LJV. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria[J]. Clinical Microbiology Reviews, 2006, 19(2): 382-402.
    [4] LI XZ, PLÉSIAT P, NIKAIDO H. The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria[J]. Clinical Microbiology Reviews, 2015, 28(2): 337-418.
    [5] VERGALLI J, ATZORI A, PAJOVIC J, DUMONT E, MALLOCI G, MASI M, VARGIU AV, WINTERHALTER M, RÉFRÉGIERS M, RUGGERONE P, PAGÈS JM. The challenge of intracellular antibiotic accumulation, a function of fluoroquinolone influx versus bacterial efflux[J]. Communications Biology, 2020, 3: 198.
    [6] XU LF, SUN XX, MA XL. Systematic review and meta-analysis of mortality of patients infected with carbapenem-resistant Klebsiella pneumoniae[J]. Annals of Clinical Microbiology and Antimicrobials, 2017, 16(1): 18.
    [7] EL-SAYED AHMED MAE, ZHONG LL, SHEN C, YANG YQ, DOI Y, TIAN GB. Colistin and its role in the era of antibiotic resistance: an extended review (2000−2019)[J]. Emerging Microbes & Infections, 2020, 9(1): 868-885.
    [8] HUSSEIN NH, AL-KADMY IMS, TAHA BM, HUSSEIN JD. Mobilized colistin resistance (mcr) genes from 1 to 10: a comprehensive review[J]. Molecular Biology Reports, 2021, 48(3): 2897-2907.
    [9] POURNARAS S, KOUMAKI V, SPANAKIS N, GENNIMATA V, TSAKRIS A. Current perspectives on tigecycline resistance in Enterobacteriaceae: susceptibility testing issues and mechanisms of resistance[J]. International Journal of Antimicrobial Agents, 2016, 48(1): 11-18.
    [10] ANYANWU MU, NWOBI OC, OKPALA COR, EZEONU IM. Mobile tigecycline resistance: an emerging health catastrophe requiring urgent one health global intervention[J]. Frontiers in Microbiology, 2022, 13: 808744.
    [11] KORNELSEN V, KUMAR A. Update on multidrug resistance efflux pumps in Acinetobacter spp.[J]. Antimicrobial Agents and Chemotherapy, 2021, 65(7): e0051421.
    [12] GLAVIER M, PUVANENDRAN D, SALVADOR D, DECOSSAS M, PHAN G, GARNIER C, FREZZA E, CECE Q, SCHOEHN G, PICARD M, TAVEAU JC, DAURY L, BROUTIN I, LAMBERT O. Antibiotic export by MexB multidrug efflux transporter is allosterically controlled by a MexA-OprM chaperone-like complex[J]. Nature Communications, 2020, 11: 4948.
    [13] BOLLA JR, HOWES AC, FIORENTINO F, ROBINSON CV. Assembly and regulation of the chlorhexidine-specific efflux pump AceI[J]. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(29): 17011-17018.
    [14] ALAV I, SUTTON JM, RAHMAN KM. Role of bacterial efflux pumps in biofilm formation[J]. Journal of Antimicrobial Chemotherapy, 2018, 73(8): 2003-2020.
    [15] GUNDOLF T, KALB R, ROSSMANITH P, MESTER P. Bacterial resistance toward antimicrobial ionic liquids mediated by multidrug efflux pumps[J]. Frontiers in Microbiology, 2022, 13: 883931.
    [16] LV LC, WAN M, WANG CZ, GAO X, YANG QW, PARTRIDGE SR, WANG Y, ZONG ZY, DOI Y, SHEN JZ, JIA PY, SONG QH, ZHANG QH, YANG J, HUANG XH, WANG MG, LIU JH. Emergence of a plasmid-encoded resistance-nodulation-division efflux pump conferring resistance to multiple drugs, including tigecycline, in Klebsiella pneumoniae[J]. mBio, 2020, 11(2): e02930-19.
    [17] SUN SJ, GAO H, LIU YD, JIN LY, WANG RB, WANG XJ, WANG Q, YIN YY, ZHANG YW, WANG H. Co-existence of a novel plasmid-mediated efflux pump with colistin resistance gene mcr in one plasmid confers transferable multidrug resistance in Klebsiella pneumoniae[J]. Emerging Microbes & Infections, 2020, 9(1): 1102-1113.
    [18] YANG XM, DONG N, CHAN EW, ZHANG R, CHEN S. Carbapenem resistance-encoding and virulence-encoding conjugative plasmids in Klebsiella pneumoniae[J]. Trends in Microbiology, 2021, 29(1): 65-83.
    [19] PAN H, JIA CH, PAUDYAL N, LI F, MAO JY, LIU X, DONG CH, ZHOU K, LIAO XY, GONG JS, FANG WH, LI XL, KEHRENBERG C, YUE M. Comprehensive Assessment of Subtyping Methods for Improved Surveillance of Foodborne Salmonella[J]. Microbiology Spectrum, 2022, 10(5): e0247922.
    [20] TANG B, SIDDIQUE A, JIA CH, ED-DRA A, WU J, LIN H, YUE M. Genome-based Risk Assessment for Foodborne Salmonella enterica from Food Animals in China: A One Health Perspective[J]. International Journal of Food Microbiology, 2023, 390: 110120.
    [21] LI Y, TENG L, XU XB, LI XM, PENG XQ, ZHOU X, DU JX, TANG YT, JIANG ZJ, WANG ZN, JIA CH, MULLER A, KEHRENBERG C, WANG HQ, WU BB, WEILL FX, YUE M. A non-typhoidal Salmonella serovar domestication accompanying enhanced niche adaptation[J]. EMBO Molecular Medicine, 2022, 14(11): e16366.
    [22] GAO X, WANG CZ, LV LC, HE XT, CAI ZP, HE WY, LI T, LIU JH. Emergence of a novel plasmid-mediated tigecycline resistance gene cluster, tmexCD4-toprJ4, in Klebsiella quasipneumoniae and Enterobacter roggenkampii[J]. Microbiology Spectrum, 2022, 10(4): e0109422.
    [23] WANG XM, WANG Y, JIANG XT, GONG XW, WANG Y, SHEN ZQ. Co-transfer of mcr-8 with blaNDM-1 or tmexCD1-toprJ1 by plasmid hybridisation[J]. International Journal of Antimicrobial Agents, 2022, 60(2): 106619.
    [24] LI Y, QIU YC, GAO Y, CHEN WB, LI CW, DAI XY, ZHANG LH. Genetic and virulence characteristics of a Raoultella planticola isolate resistant to carbapenem and tigecycline[J]. Scientific Reports, 2022, 12: 3858.
    [25] XIAO T, PENG K, CHEN Q, HOU XQ, HUANG WF, LV H, YANG XR, LEI GP, LI RC. Coexistence of tmexCD-toprJ, blaNDM-1, and blaIMP-4 in one plasmid carried by clinical Klebsiella spp.[J]. Microbiology Spectrum, 2022, 10(3): e0054922.
    [26] LI RC, PENG K, XIAO X, LIU Y, PENG DX, WANG ZQ. Emergence of a multidrug resistance efflux pump with carbapenem resistance gene blaVIM-2 in a Pseudomonas putida megaplasmid of migratory bird origin[J]. The Journal of Antimicrobial Chemotherapy, 2021, 76(6): 1455-1458.
    [27] XU LN, WAN F, FU H, TANG B, RUAN Z, XIAO YH, LUO QX. Emergence of colistin resistance gene mcr–10 in Enterobacterales isolates recovered from fecal samples of chickens, slaughterhouse workers, and a nearby resident[J]. Microbiology Spectrum, 2022, 10(2): e0041822.
    [28] WU YC, DONG N, CAI C, ZHANG R, CHEN S. Hospital wastewater as a reservoir for the tigecycline resistance gene cluster tmexCD-toprJ[J]. The Lancet Microbe, 2023, 4(3): e134.
    [29] LIU CC, WU YC, FANG YF, SANG Z, HUANG L, DONG N, ZENG Y, LU JY, ZHANG R, CHEN GX. Emergence of an ST1326(CG258) multi-drug resistant Klebsiella pneumoniae co-harboring mcr-8.2, ESBL genes, and the resistance-nodulation-division efflux pump gene cluster tmexCD1-toprJ1 in China[J]. Frontiers in Microbiology, 2022, 13: 800993.
    [30] WANG XM, SUN NY, LIU X, LI F, SUN JJ, HUANG JH, LI RC, WANG LP. Small clone dissemination of tmexCD1-toprJ1-carrying Klebsiella pneumoniae isolates in a chicken farm[J]. Journal of Global Antimicrobial Resistance, 2022, 29: 105-112.
    [31] PENG K, WANG Q, YIN Y, LI Y, LIU Y, WANG MZ, QIN SS, WANG ZQ, LI RC. Plasmids shape the current prevalence of tmexCD1-toprJ1 among Klebsiella pneumoniae in food production chains[J]. mSystems, 2021, 6(5): e70221.
    [32] QIN SS, PENG JK, DENG RP, PENG K, YAN TT, CHEN FF, LI RC. Identification of two plasmids coharboring carbapenemase genes and tmexCD1-toprJ1 in clinical Klebsiella pneumoniae ST2667[J]. Antimicrobial Agents and Chemotherapy, 2021, 65(6): e00625-21.
    [33] YANG XM, YE LW, CHAN EWC, ZHANG R, CHEN S. Characterization of an IncFIB/IncHI1B plasmid encoding efflux pump TMexCD1-TOprJ1 in a clinical tigecycline- and carbapenem-resistant Klebsiella pneumoniae strain[J]. Antimicrobial Agents and Chemotherapy, 2021, 65(4): e02340-20.
    [34] FU YL, CHEN YQ, LIU DJ, YANG DW, LIU ZH, WANG YY, WANG JY, WANG XY, XU XY, LI X, HE JJ, JIANG JY, ZHAI WS, HUANG LL, HE T, XIA X, CAI C, WANG Y, JIANG HY. Abundance of tigecycline resistance genes and association with antibiotic residues in Chinese livestock farms[J]. Journal of Hazardous Materials, 2021, 409: 124921.
    [35] LIU YY, GAO X, HE XT, LV LC, JIAO YX, YU RY, LIU JH. Emergence of the tigecycline resistance gene cluster tmexCD1-toprJ1 in an IncC plasmid and Citrobacter portucalensis[J]. Journal of Antimicrobial Chemotherapy, 2022, 77(7): 2030-2033.
    [36] WAN M, GAO X, LV LC, CAI ZP, LIU JH. IS26 mediates the acquisition of tigecycline resistance gene cluster tmexCD1-toprJ1 by IncHI1B-FIB plasmids in Klebsiella pneumoniae and Klebsiella quasipneumoniae from food market sewage[J]. Antimicrobial Agents and Chemotherapy, 2021, 65(3): e02178-20.
    [37] HE RW, YANG YQ, WU YP, ZHONG LL, YANG YX, CHEN GP, QIN MY, LIANG XX, EL-GAWAD EL-SAYED AHMED MA, LIN MM, YAN B, XIA Y, DAI M, CHEN HT, TIAN GB. Characterization of a plasmid-encoded resistance-nodulation-division efflux pump in Klebsiella pneumoniae and Klebsiella quasipneumoniae from patients in China[J]. Antimicrobial Agents and Chemotherapy, 2021, 65(2): e02075-20.
    [38] LIU YL, LIN YQ, WANG ZW, HU NY, LIU Q, ZHOU WK, LI XZ, HU LH, GUO J, HUANG XT, ZENG LB. Molecular mechanisms of colistin resistance in Klebsiella pneumoniae in a tertiary care teaching hospital[J]. Frontiers in Cellular and Infection Microbiology, 2021, 11: 673503.
    [39] SUN SJ, WANG Q, JIN LY, GUO YF, YIN YY, WANG RB, BI L, ZHANG RF, HAN YG, WANG H. Identification of multiple transfer units and novel subtypes of tmexCD-toprJ gene clusters in clinical carbapenem-resistant Enterobacter cloacae and Klebsiella oxytoca[J]. Journal of Antimicrobial Chemotherapy, 2022, 77(3): 625-632.
    [40] HIRABAYASHI A, HA VTT, van NGUYEN A, NGUYEN ST, SHIBAYAMA K, SUZUKI M. Emergence of a plasmid-borne tigecycline resistance in Klebsiella pneumoniae in Vietnam[J]. Journal of Medical Microbiology, 2021, 70(3): https://doi.org/10.1099/jmm.0.001320.
    [41] WANG YJ, ZHU B, LIU M, DONG XT, MA JP, LI XF, CHENG F, GUO JZ, LU SM, WAN FR, HAO YY, MA WS, HAO MJ, CHEN L. Characterization of IncHI1B plasmids encoding efflux pump TmexCD2-ToprJ2 in carbapenem-resistant Klebsiella variicola, Klebsiella quasipneumoniae, and Klebsiella michiganensis strains[J]. Frontiers in Microbiology, 2021, 12: 759208.
    [42] WANG CZ, GAO X, YANG QW, LV LC, WAN M, YANG J, CAI ZP, LIU JH. A novel transferable resistance-nodulation-division pump gene cluster, tmexCD2-toprJ2, confers tigecycline resistance in Raoultella ornithinolytica[J]. Antimicrobial Agents and Chemotherapy, 2021, 65(4): e02229-20.
    [43] WU YC, DONG N, CAI C, ZENG Y, LU JY, LIU CC, WANG HY, ZHANG YY, HUANG L, ZHAI WS, SHAO DY, LI RC, LIU DJ, CHEN S, ZHANG R. Aeromonas spp. from hospital sewage act as a reservoir of genes resistant to last-line antibiotics[J]. Drug Resistance Updates, 2023, 67: 100925.
    [44] WANG Q, PENG K, LIU Y, XIAO X, WANG ZQ, LI RC. Characterization of TMexCD3-TOprJ3, an RND-type efflux system conferring resistance to tigecycline in Proteus mirabilis, and its associated integrative conjugative element[J]. Antimicrobial Agents and Chemotherapy, 2021, 65(7): e271220.
    [45] HIRABAYASHI A, DAO TD, TAKEMURA T, HASEBE F, TRANG LT, THANH NH, TRAN HH, SHIBAYAMA K, KASUGA I, SUZUKI M. A transferable IncC-IncX3 hybrid plasmid cocarrying blaNDM-4, tet(X), and tmexCD3-toprJ3 confers resistance to carbapenem and tigecycline[J]. mSphere, 2021, 6(4): e0059221.
    [46] WANG CZ, GAO X, LV LC, CAI ZP, YANG J, LIU JH. Novel tigecycline resistance gene cluster tnfxB3-tmexCD3-toprJ1b in Proteus spp. and Pseudomonas aeruginosa, co-existing with Tet(X6) on an SXT/R391 integrative and conjugative element[J]. Journal of Antimicrobial Chemotherapy, 2021, 76(12): 3159-3167.
    [47] FROST LS, LEPLAE R, SUMMERS AO, TOUSSAINT A. Mobile genetic elements: the agents of open source evolution[J]. Nature Reviews Microbiology, 2005, 3(9): 722-732.
    [48] LIU C, DU PC, YANG P, ZHENG JJ, YI J, LU M, SHEN N. Emergence and inter- and intrahost evolution of pandrug-resistant Klebsiella pneumoniae coharboring tmexCD1-toprJ1, blaNDM-1, and blaKPC-2[J]. Microbiology Spectrum, 2023, 11(2): e0278622.
    [49] CARROLL AC, WONG A. Plasmid persistence: costs, benefits, and the plasmid paradox[J]. Canadian Journal of Microbiology, 2018, 64(5): 293-304.
    [50] ZHANG YX, LI ZY, XU X, PENG X. Transposon mutagenesis in oral streptococcus[J]. Journal of Oral Microbiology, 2022, 14(1): 2104951.
    [51] 吴小磊, 贾程皓, 王剑峰, 王雷杰, 乐敏. DNA聚合酶IV:抗细菌的潜在药靶[J]. 微生物学通报, 2022, 49(12): 5342-5358.WU XL, JIA CH, WANG JF, WANG LJ, YUE M. DNA polymerase IV - a potential drug target against bacteria[J]. Microbiology China, 2022, 49(12): 5342-5358(in Chinese).
    [52] KUMAR N, SU CC, CHOU TH, RADHAKRISHNAN A, DELMAR JA, RAJASHANKAR KR, YU EW. Crystal structures of the Burkholderia multivorans hopanoid transporter HpnN[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(25): 6557-6562.
    [53] YONEHARA R, YAMASHITA E, NAKAGAWA A. Crystal structures of OprN and OprJ, outer membrane factors of multidrug tripartite efflux pumps of Pseudomonas aeruginosa[J]. Proteins: Structure, Function, and Bioinformatics, 2016, 84(6): 759-769.
    [54] WANG Z, FAN GZ, HRYC CF, BLAZA JN, SERYSHEVA II, SCHMID MF, CHIU W, LUISI BF, DU DJ. An allosteric transport mechanism for the AcrAB-TolC multidrug efflux pump[J]. eLife, 2017, 6: 24905.
    [55] TSUTSUMI K, YONEHARA R, ISHIZAKA-IKEDA E, MIYAZAKI N, MAEDA S, IWASAKI K, NAKAGAWA A, YAMASHITA E. Structures of the wild-type MexAB-OprM tripartite pump reveal its complex formation and drug efflux mechanism[J]. Nature Communications, 2019, 10: 1520.
    [56] 方家豪, 曹雨虹, 何宇臻, 洪战英, 柴逸峰. 膜蛋白稳定技术及其在药物筛选中的应用进展[J]. 药学学报, 2021, 56(9): 2325-2334. FANG JH, CAO YH, HE YZ, HONG ZY, CHAI YF. Advancements in stabilization technologies for membrane protein and its application in drug screening[J]. Acta Pharmaceutica Sinica, 2021, 56(9): 2325-2334(in Chinese).
    [57] DOUGHTY DM, COLEMAN ML, HUNTER RC, SESSIONS AL, SUMMONS RE, NEWMAN DK. The RND-family transporter, HpnN, is required for hopanoid localization to the outer membrane of Rhodopseudomonas palustris TIE-1[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(45): E1045-E1051.
    [58] KLENOTIC PA, MOSENG MA, MORGAN CE, YU EW. Structural and functional diversity of resistance-nodulation-cell division transporters[J]. Chemical Reviews, 2021, 121(9): 5378-5416.
    [59] MCEWEN SA, COLLIGNON PJ. Antimicrobial resistance: a one health perspective[J]. Microbiology Spectrum, 2018, 6(2): http://10.1128/microbiolspec.ARBA-0009-2017.
    [60] SINCLAIR JR. Importance of a One Health approach in advancing global health security and the sustainable development goals[J]. Revue Scientifique et Technique De L’OIE, 2019, 38(1): 145-154.
    [61] PENG X, ED-DRA A, YUE M. Whole genome sequencing for the risk assessment of probiotic lactic acid bacteria[J]. Critical Reviews in Food Science and Nutrition, 2022, 13: 1-19.
    [62] ELBEDIWI M, LI Y, PAUDYAL N, PAN H, LI XL, XIE SH, RAJKOVIC A, FENG YJ, FANG WH, RANKIN SC, YUE M. Global burden of colistin-resistant bacteria: mobilized colistin resistance genes study (1980−2018)[J]. Microorganisms, 2019, 7(10): 461.
    [63] 武淑霞, 刘宏斌, 黄宏坤, 雷秋良, 王洪媛, 翟丽梅, 刘申, 张英, 胡钰. 我国畜禽养殖粪污产生量及其资源化分析[J]. 中国工程科学, 2018, 20(5): 103-111. WU SX, LIU HB, HUANG HK, LEI QL, WANG HY, ZHAI LM, LIU S, ZHANG Y, HU Y. Analysis on the amount and utilization of manure in livestock and poultry breeding in China[J]. Engineering Science, 2018, 20(5): 103-111(in Chinese).
    [64] LI Y, ED-DRA A, TANG B, KANG XM, MÜLLER A, KEHRENBERG C, JIA CH, PAN H, YANG H, YUE M. Higher tolerance of predominant Salmonella serovars circulating in the antibiotic-free feed farms to environmental stresses[J]. Journal of Hazardous Materials, 2022, 438: 129476.
    [65] KARKMAN A, PÄRNÄNEN K, LARSSON DGJ. Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments[J]. Nature Communications, 2019, 10: 80.
    [66] EZZARIAI A, HAFIDI M, KHADRA A, AEMIG Q, EL FELS L, BARRET M, MERLINA G, PATUREAU D, PINELLI E. Human and veterinary antibiotics during composting of sludge or manure: global perspectives on persistence, degradation, and resistance genes[J]. Journal of Hazardous Materials, 2018, 359: 465-481.
    [67] 刘海洋. 污水中典型抗生素、耐药菌及耐药基因的分布及其电催化降解研究[D]. 长春: 东北师范大学博士学位论文, 2020. LIU HY. Distribution and electrocatalytic degradation of typical antibiotics, drug-resistant bacteria and drug-resistant genes in sewage[D]. Changchun: Doctoral Dissertation of Northeast Normal University, 2020(in Chinese).
    [68] GLASSER NR, KERN SE, NEWMAN DK. Phenazine redox cycling enhances anaerobic survival in Pseudomonas aeruginosaby facilitating generation of ATP and a proton-motive force[J]. Molecular Microbiology, 2014, 92(2): 399-412.
    [69] XIAO X, HUAN QM, HUANG YH, LIU Y, LI RC, XU XL, WANG ZQ. Metformin reverses tmexCD1-toprJ1- and Tet(A)-mediated high-level tigecycline resistance in K. pneumoniae[J]. Antibiotics, 2022, 11(2): 162.
    [70] SEYEDHOSSEINI GHAHEH H, DAMAVANDI MS, SADEGHI P, MASSAH AR, ASL TH, SALARI-JAZI A, HEJAZI SH. Targeting and ultrabroad insight into molecular basis of resistance-nodulation-cell division efflux pumps[J]. Scientific Reports, 2022, 12: 16130.
    [71] DAVIN-REGLI A, PAGES JM, FERRAND A. Clinical status of efflux resistance mechanisms in Gram-negative bacteria[J]. Antibiotics, 2021, 10(9): 1117.
    [72] VERMA P, TIWARI V. Targeting outer membrane protein component AdeC for the discovery of efflux pump inhibitor against AdeABC efflux pump of multidrug resistant Acinetobacter baumannii[J]. Cell Biochemistry and Biophysics, 2018, 76(3): 391-400.
    [73] AYHAN DH, TAMER YT, AKBAR M, BAILEY SM, WONG M, DALY SM, GREENBERG DE, TOPRAK E. Sequence-specific targeting of bacterial resistance genes increases antibiotic efficacy[J]. PLoS Biology, 2016, 14(9): e1002552.
    [74] NAGANO K, NIKAIDO H. Kinetic behavior of the major multidrug efflux pump AcrB of Escherichia coli[J]. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(14): 5854-5858.
    [75] NIKAIDO H, PAGÈS JM. Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria[J]. FEMS Microbiology Reviews, 2012, 36(2): 340-363.
    Cited by
    Comments
    Comments
    分享到微博
    Submit
Get Citation

SUN Jingdu, JIA Chenghao, TANG Biao, ZHAO Guoping, YUE Min. Research progress in a novel mobile RND efflux pump TMexCD-TOprJ. [J]. Acta Microbiologica Sinica, 2023, 63(11): 4101-4117

Copy
Share
Article Metrics
  • Abstract:
  • PDF:
  • HTML:
  • Cited by:
History
  • Received:March 20,2023
  • Revised:May 24,2023
  • Online: November 03,2023
  • Published: November 04,2023
Article QR Code