{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T03:14:49Z","timestamp":1792120489200,"version":"4.4.0"},"reference-count":87,"publisher":"Akademiai Kiado Zrt.","issue":"2","funder":[{"name":"Thailand Science Research and Innovation (TSRI), Chulabhorn Research Institute","award":["49892\/4759806"],"award-info":[{"award-number":["49892\/4759806"]}]}],"content-domain":{"domain":["akjournals.com"],"crossmark-restriction":true},"short-container-title":["AMicr"],"published-print":{"date-parts":[[2025,6,20]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p><jats:italic>Stenotrophomonas maltophilia<\/jats:italic> has emerged as an opportunistic pathogen originating from the environments, causing nosocomial infections, particularly in immunocompromised individuals and patients with cystic fibrosis. Although this microorganism exhibits low virulence, its infections are associated with high morbidity and mortality rates. <jats:italic>S. maltophilia<\/jats:italic> is intrinsically resistant to many antimicrobial agents used in clinical practices, therefore, posing significant treatment challenges. The multidrug resistance in <jats:italic>S. maltophilia<\/jats:italic> results from a combination of intrinsic, adaptive, and acquired mechanisms. <jats:italic>S. maltophilia<\/jats:italic> genome carries an array of genes encoding multidrug efflux pumps, which are key contributors to its broad-spectrum antibiotic resistance by expelling a wide range of drugs and reducing their intracellular concentrations to nontoxic levels. The majority of these efflux pumps belong to the resistance-nodulation-cell division (RND) family, while a lesser fraction is classified under the major facilitator superfamily (MFS) and the adenosine triphosphate binding cassette (ABC) family. In terms of function, substrate specificity, and complex gene regulation, these multidrug efflux pumps contribute not only to the survival of <jats:italic>S. maltophilia<\/jats:italic> under antibiotic stress but also to its resilience against other chemical challenges, including oxidative stress-generating substances and biocides. The roles of certain efflux pump systems in acquired and adaptive antibiotic resistance, as well as their potential applications as drug targets to enhance the efficacy of routinely used antibiotics through the use of small molecules capable of functioning as efflux pump inhibitors, are also discussed. A deeper understanding of these\u00a0mechanisms can contribute to the more effective management against antibiotic-resistant <jats:italic>S.\u00a0maltophilia<\/jats:italic>.<\/jats:p>","DOI":"10.1556\/030.2025.02578","type":"journal-article","created":{"date-parts":[[2025,5,22]],"date-time":"2025-05-22T14:28:44Z","timestamp":1747924124000},"page":"81-92","update-policy":"https:\/\/doi.org\/10.1556\/policypage.crossmark.crossref.2","source":"Crossref","is-referenced-by-count":8,"title":["Efflux pump systems as key contributors to\u00a0multidrug resistance in Stenotrophomonas maltophilia: Physiological roles and gene regulation"],"prefix":"10.1556","volume":"72","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8744-4963","authenticated-orcid":true,"given":"Paiboon","family":"Vattanaviboon","sequence":"first","affiliation":[{"name":"Laboratory of Biotechnology, Chulabhorn Research Institute, Bangkok 10210, Thailand"},{"name":"Center of Excellence on Environmental Health and Toxicology (EHT), OPS, MHESI, Bangkok 10400, Thailand"},{"name":"Program in Applied Biological Science: Environmental Health, Chulabhorn Graduate Institute, Bangkok 10210, Thailand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Punyawee","family":"Dulyayangkul","sequence":"additional","affiliation":[{"name":"Laboratory of Biotechnology, Chulabhorn Research Institute, Bangkok 10210, Thailand"},{"name":"Center of Excellence on Environmental Health and Toxicology (EHT), OPS, MHESI, Bangkok 10400, Thailand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Skorn","family":"Mongkolsuk","sequence":"additional","affiliation":[{"name":"Laboratory of Biotechnology, Chulabhorn Research Institute, Bangkok 10210, Thailand"},{"name":"Center of Excellence on Environmental Health and Toxicology (EHT), OPS, MHESI, Bangkok 10400, Thailand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nisanart","family":"Charoenlap","sequence":"additional","affiliation":[{"name":"Laboratory of Biotechnology, Chulabhorn Research Institute, Bangkok 10210, Thailand"},{"name":"Center of Excellence on Environmental Health and Toxicology (EHT), OPS, MHESI, Bangkok 10400, Thailand"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"425","reference":[{"key":"B1","series-title":"Lancet Infect Dis","first-page":"312","article-title":"Stenotrophomonas maltophilia: an emerging opportunist human pathogen","volume":"9","author":"Looney WJ","year":"2009","unstructured":"Looney WJ, Narita M, Muhlemann K. Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 2009; 9: 312\u2013323."},{"key":"B2","series-title":"Clin Microbiol Rev","article-title":"Advances in the microbiology of Stenotrophomonas maltophilia","volume":"34","author":"Brooke JS","year":"2021","unstructured":"Brooke JS. Advances in the microbiology of Stenotrophomonas maltophilia. Clin Microbiol Rev 2021; 34: e0003019."},{"key":"B3","series-title":"Eur J Clin Microbiol Infect Dis","first-page":"1285","article-title":"Stenotrophomonas maltophilia in people with cystic fibrosis: a\u00a0systematic review of prevalence, risk factors and management","volume":"42","author":"Terlizzi V","year":"2023","unstructured":"Terlizzi V, Tomaselli M, Giacomini G, Dalpiaz I, Chiappini E. Stenotrophomonas maltophilia in people with cystic fibrosis: a\u00a0systematic review of prevalence, risk factors and management. Eur J Clin Microbiol Infect Dis 2023; 42: 1285\u20131296."},{"key":"B4","series-title":"Infect Drug Resist","first-page":"3881","article-title":"Risk factors for mortality in hospitalized patients with Stenotrophomonas maltophilia bacteremia","volume":"15","author":"Jian J","year":"2022","unstructured":"Jian J, Xie Z, Chen L. Risk factors for mortality in hospitalized patients with Stenotrophomonas maltophilia bacteremia. Infect Drug Resist 2022; 15: 3881\u20133886."},{"key":"B5","series-title":"BMC Infect Dis","first-page":"754","article-title":"Risk factors for mortality in patients with Stenotrophomonas maltophilia bacteremia and clinical impact of quinolone-resistant strains","volume":"19","author":"Kim EJ","year":"2019","unstructured":"Kim EJ, Kim YC, Ahn JY, Jeong SJ, Ku NS, Choi JY, et\u00a0al. Risk factors for mortality in patients with Stenotrophomonas maltophilia bacteremia and clinical impact of quinolone-resistant strains. BMC Infect Dis 2019; 19: 754."},{"key":"B6","series-title":"Infect Drug Resist","first-page":"1559","article-title":"Stenotrophomonas maltophilia infections: clinical characteristics and factors associated with mortality of hospitalized patients","volume":"13","author":"Insuwanno W","year":"2020","unstructured":"Insuwanno W, Kiratisin P, Jitmuang A. Stenotrophomonas maltophilia infections: clinical characteristics and factors associated with mortality of hospitalized patients. Infect Drug Resist 2020; 13: 1559\u20131566."},{"key":"B7","series-title":"Infection","first-page":"205","article-title":"The clinical impact of Stenotrophomonas maltophilia bacteremia on the 30-day mortality rate in patients with hematologic disorders: a single-institution experience","volume":"48","author":"Bao H","year":"2020","unstructured":"Bao H, Qiao Y, Liu D, Chen J, Wu X, Hu X, et\u00a0al. The clinical impact of Stenotrophomonas maltophilia bacteremia on the 30-day mortality rate in patients with hematologic disorders: a single-institution experience. Infection 2020; 48: 205\u2013212."},{"key":"B8","series-title":"PLoS One","article-title":"Risk factors associated with Stenotrophomonas maltophilia bacteremia: a matched case-control study","volume":"10","author":"Sumida K","year":"2015","unstructured":"Sumida K, Chong Y, Miyake N, Akahoshi T, Yasuda M, Shimono N, et\u00a0al. Risk factors associated with Stenotrophomonas maltophilia bacteremia: a matched case-control study. PLoS One 2015; 10: e0133731."},{"key":"B9","series-title":"Genome Biol","first-page":"R74","article-title":"The complete genome, comparative and functional\u00a0analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants","volume":"9","author":"Crossman LC","year":"2008","unstructured":"Crossman LC, Gould VC, Dow JM, Vernikos GS, Okazaki A, Sebaihia M, et\u00a0al. The complete genome, comparative and functional\u00a0analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 2008; 9: R74."},{"key":"B10","series-title":"J Glob Antimicrob Resist","first-page":"186","article-title":"Characteristic antimicrobial resistance of clinically isolated Stenotrophomonas maltophilia CYZ via complete genome sequence","volume":"23","author":"Ma J","year":"2020","unstructured":"Ma J, Feng J, Shan Y, Zhao Y, Qiao H, Xie L, et\u00a0al. Characteristic antimicrobial resistance of clinically isolated Stenotrophomonas maltophilia CYZ via complete genome sequence. J Glob Antimicrob Resist 2020; 23: 186\u2013193."},{"key":"B11","series-title":"Front Microbiol","first-page":"658","article-title":"Antibiotic resistance in the opportunistic pathogen Stenotrophomonas maltophilia","volume":"6","author":"Sanchez MB","year":"2015","unstructured":"Sanchez MB. Antibiotic resistance in the opportunistic pathogen Stenotrophomonas maltophilia. Front Microbiol 2015; 6: 658."},{"key":"B12","series-title":"Int J Antimicrob Agents","first-page":"230","article-title":"Stenotrophomonas maltophilia resistance to trimethoprim\/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron","volume":"37","author":"Hu LF","year":"2011","unstructured":"Hu LF, Chang X, Ye Y, Wang ZX, Shao YB, Shi W, et\u00a0al. 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Novel mechanisms of efflux-mediated levofloxacin resistance and reduced amikacin susceptibility in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2020; 65."},{"key":"B15","series-title":"Antimicrob Agents Chemother","first-page":"3386","article-title":"Cloning and characterization of SmeT, a repressor of the Stenotrophomonas maltophilia multidrug efflux pump SmeDEF","volume":"46","author":"Sanchez P","year":"2002","unstructured":"Sanchez P, Alonso A, Martinez JL. Cloning and characterization of SmeT, a repressor of the Stenotrophomonas maltophilia multidrug efflux pump SmeDEF. Antimicrob Agents Chemother 2002; 46: 3386\u20133393."},{"key":"B16","series-title":"Antimicrob Agents Chemother","article-title":"Overexpression of the efflux pumps SmeVWX and SmeDEF is a major cause of resistance to co-trimoxazole in Stenotrophomonas maltophilia","volume":"62","author":"Sanchez MB","year":"2018","unstructured":"Sanchez MB, Martinez JL. Overexpression of the efflux pumps SmeVWX and SmeDEF is a major cause of resistance to co-trimoxazole in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2018; 62."},{"key":"B17","series-title":"Sci Rep","first-page":"4917","article-title":"Involvement of the RND efflux pump transporter SmeH in the acquisition of resistance to ceftazidime in Stenotrophomonas maltophilia","volume":"9","author":"Blanco P","year":"2019","unstructured":"Blanco P, Corona F, Martinez JL. Involvement of the RND efflux pump transporter SmeH in the acquisition of resistance to ceftazidime in Stenotrophomonas maltophilia. Sci Rep 2019; 9: 4917."},{"key":"B18","series-title":"Antimicrob Agents Chemother","article-title":"Mutations in ribosomal protein rpla or treatment with ribosomal acting antibiotics activates production of aminoglycoside efflux pump SmeYZ in Stenotrophomonas maltophilia","volume":"64","author":"Calvopina K","year":"2020","unstructured":"Calvopina K, Dulyayangkul P, Avison MB. 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Antimicrob Agents Chemother 2002; 46: 333\u2013343."},{"key":"B28","series-title":"Antimicrob Agents Chemother","first-page":"3079","article-title":"Cloning and characterization of SmeDEF, a\u00a0novel multidrug efflux pump from Stenotrophomonas maltophilia","volume":"44","author":"Alonso A","year":"2000","unstructured":"Alonso A, Martinez JL. Cloning and characterization of SmeDEF, a\u00a0novel multidrug efflux pump from Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2000; 44: 3079\u20133086."},{"key":"B29","series-title":"Antimicrob Agents Chemother","first-page":"287","article-title":"Multiple antibiotic resistance in Stenotrophomonas maltophilia: involvement of a multidrug efflux system","volume":"44","author":"Zhang L","year":"2000","unstructured":"Zhang L, Li XZ, Poole K. Multiple antibiotic resistance in Stenotrophomonas maltophilia: involvement of a multidrug efflux system. Antimicrob Agents Chemother 2000; 44: 287\u2013293."},{"key":"B30","series-title":"J Antimicrob Chemother","first-page":"2225","article-title":"Overexpression of SmeGH contributes to the acquired MDR of Stenotrophomonas maltophilia","volume":"74","author":"Li LH","year":"2019","unstructured":"Li LH, Zhang MS, Wu CJ, Lin YT, Yang TC. Overexpression of SmeGH contributes to the acquired MDR of Stenotrophomonas maltophilia. J Antimicrob Chemother 2019; 74: 2225\u20132229."},{"key":"B31","series-title":"Antimicrob Agents Chemother","first-page":"655","article-title":"Coordinate hyperproduction of SmeZ and SmeJK efflux pumps extends drug resistance in Stenotrophomonas maltophilia","volume":"57","author":"Gould VC","year":"2013","unstructured":"Gould VC, Okazaki A, Avison MB. Coordinate hyperproduction of SmeZ and SmeJK efflux pumps extends drug resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2013; 57: 655\u2013657."},{"key":"B32","series-title":"Antimicrob Agents Chemother","first-page":"2405","article-title":"SmeOP-TolCSm efflux pump contributes to the multidrug resistance of Stenotrophomonas maltophilia","volume":"58","author":"Lin CW","year":"2014","unstructured":"Lin CW, Huang YW, Hu RM, Yang TC. SmeOP-TolCSm efflux pump contributes to the multidrug resistance of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2014; 58: 2405\u20132408."},{"key":"B33","series-title":"Antimicrob Agents Chemother","first-page":"5826","article-title":"Contribution of resistance-nodulation-division efflux pump operon smeU1-V-W-U2-X to multidrug resistance of Stenotrophomonas maltophilia","volume":"55","author":"Chen CH","year":"2011","unstructured":"Chen CH, Huang CC, Chung TC, Hu RM, Huang YW, Yang TC. Contribution of resistance-nodulation-division efflux pump operon smeU1-V-W-U2-X to multidrug resistance of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2011; 55: 5826\u20135833."},{"key":"B34","series-title":"Antimicrob Agents Chemother","first-page":"4067","article-title":"The SmeYZ efflux pump of Stenotrophomonas maltophilia contributes to drug resistance, virulence-related characteristics, and virulence in mice","volume":"59","author":"Lin YT","year":"2015","unstructured":"Lin YT, Huang YW, Chen SJ, Chang CW, Yang TC. The SmeYZ efflux pump of Stenotrophomonas maltophilia contributes to drug resistance, virulence-related characteristics, and virulence in mice. Antimicrob Agents Chemother 2015; 59: 4067\u20134073."},{"key":"B35","series-title":"J Antimicrob Chemother","first-page":"2498","article-title":"Characterization of a major facilitator superfamily (MFS) tripartite efflux pump EmrCABsm from Stenotrophomonas maltophilia","volume":"68","author":"Huang YW","year":"2013","unstructured":"Huang YW, Hu RM, Chu FY, Lin HR, Yang TC. 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J Antimicrob Chemother 2016; 71: 2990\u20132991."},{"key":"B37","series-title":"PLoS One","article-title":"An inducible fusaric acid tripartite efflux pump contributes to the fusaric acid resistance in Stenotrophomonas maltophilia","volume":"7","author":"Hu RM","year":"2012","unstructured":"Hu RM, Liao ST, Huang CC, Huang YW, Yang TC. An inducible fusaric acid tripartite efflux pump contributes to the fusaric acid resistance in Stenotrophomonas maltophilia. PLoS One 2012; 7: e51053."},{"key":"B38","series-title":"J Antimicrob Chemother","first-page":"3221","article-title":"MacABCsm, an ABC-type tripartite efflux pump of Stenotrophomonas maltophilia involved in drug resistance, oxidative and envelope stress tolerances and biofilm formation","volume":"69","author":"Lin YT","year":"2014","unstructured":"Lin YT, Huang YW, Liou RS, Chang YC, Yang TC. 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Antimicrob Agents Chemother 2020; 64."},{"key":"B40","series-title":"Antibiotics (Basel)","article-title":"Role of RND efflux pumps in drug resistance of cystic fibrosis pathogens","volume":"10","author":"Scoffone VC","year":"2021","unstructured":"Scoffone VC, Trespidi G, Barbieri G, Irudal S, Perrin E, Buroni S. Role of RND efflux pumps in drug resistance of cystic fibrosis pathogens. Antibiotics (Basel) 2021; 10."},{"key":"B41","series-title":"Trends Biochem Sci","first-page":"369","article-title":"Histidine kinases and response regulator proteins in two-component signaling systems","volume":"26","author":"West AH","year":"2001","unstructured":"West AH, Stock AM. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 2001; 26: 369\u2013376."},{"key":"B42","series-title":"J Biol Chem","first-page":"1448","article-title":"Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli","volume":"280","author":"Yamamoto K","year":"2005","unstructured":"Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R, Ishihama A. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 2005; 280: 1448\u20131456."},{"key":"B43","series-title":"J Bacteriol","first-page":"3367","article-title":"Characterization of the induction and cellular role of the BaeSR two-component envelope stress response of Escherichia coli","volume":"193","author":"Leblanc SK","year":"2011","unstructured":"Leblanc SK, Oates CW, Raivio TL. Characterization of the induction and cellular role of the BaeSR two-component envelope stress response of Escherichia coli. 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J\u00a0Antimicrob Chemother 2004; 53: 518\u2013521."},{"key":"B46","series-title":"Ann Lab Med","first-page":"38","article-title":"Expression of Sme efflux pumps and multilocus sequence typing in clinical isolates of Stenotrophomonas maltophilia","volume":"32","author":"Cho HH","year":"2012","unstructured":"Cho HH, Sung JY, Kwon KC, Koo SH. Expression of Sme efflux pumps and multilocus sequence typing in clinical isolates of Stenotrophomonas maltophilia. Ann Lab Med 2012; 32: 38\u201343."},{"key":"B47","series-title":"Antimicrob Agents Chemother","first-page":"3497","article-title":"SmeDEF multidrug efflux pump contributes to intrinsic multidrug resistance in Stenotrophomonas maltophilia","volume":"45","author":"Zhang L","year":"2001","unstructured":"Zhang L, Li XZ, Poole K. SmeDEF multidrug efflux pump contributes to intrinsic multidrug resistance in Stenotrophomonas maltophilia. 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Antimicrob Agents Chemother 2018; 62."},{"key":"B63","series-title":"Antimicrob Agents Chemother","article-title":"Vitamin K(3) induces the expression of the Stenotrophomonas maltophilia SmeVWX multidrug efflux pump","volume":"61","author":"Blanco P","year":"2017","unstructured":"Blanco P, Corona F, Sanchez MB, Martinez JL. Vitamin K(3) induces the expression of the Stenotrophomonas maltophilia SmeVWX multidrug efflux pump. Antimicrob Agents Chemother 2017; 61."},{"key":"B64","series-title":"Antonie Van Leeuwenhoek","first-page":"809","article-title":"Inactivation of ahpC renders Stenotrophomonas maltophilia resistant to the disinfectant hydrogen peroxide","volume":"112","author":"Charoenlap N","year":"2019","unstructured":"Charoenlap N, Jiramonai L, Chittrakanwong J, Tunsakul N, Mongkolsuk S, Vattanaviboon P. Inactivation of ahpC renders Stenotrophomonas maltophilia resistant to the disinfectant hydrogen peroxide. Antonie Van Leeuwenhoek 2019; 112: 809\u2013814."},{"key":"B65","series-title":"FEMS Microbiol Lett","first-page":"372","article-title":"SoxR-dependent regulation of sodA1 and its impact on Stenotrophomonas maltophilia survival under external oxidative stress","author":"Giengkam S","year":"2025","unstructured":"Giengkam S, Charoenlap N, Whangsuk W, Bhinija K, Mongkolsuk S, Vattanaviboon P. SoxR-dependent regulation of sodA1 and its impact on Stenotrophomonas maltophilia survival under external oxidative stress. FEMS Microbiol Lett 2025: 372."},{"key":"B66","series-title":"Int J Mol Sci","article-title":"Roles of the two-MnSOD system of Stenotrophomonas maltophilia in the alleviation of superoxide stress","volume":"20","author":"Jair HW","year":"2019","unstructured":"Jair HW, Lu HF, Huang YW, Pan SY, Lin IL, Huang HH, et\u00a0al. Roles of the two-MnSOD system of Stenotrophomonas maltophilia in the alleviation of superoxide stress. Int J Mol Sci 2019; 20."},{"key":"B67","series-title":"J Biomed Sci","first-page":"37","article-title":"Protection from hydrogen peroxide stress relies mainly on AhpCF and KatA2 in Stenotrophomonas maltophilia","volume":"27","author":"Li LH","year":"2020","unstructured":"Li LH, Shih YL, Huang JY, Wu CJ, Huang YW, Huang HH, et\u00a0al. Protection from hydrogen peroxide stress relies mainly on AhpCF and KatA2 in Stenotrophomonas maltophilia. J Biomed Sci 2020; 27: 37."},{"key":"B68","series-title":"EMBO J","first-page":"1056","article-title":"Spacing of promoter elements regulates the basal expression of the soxS gene and converts SoxR from a transcriptional activator into a repressor","volume":"16","author":"Hidalgo E","year":"1997","unstructured":"Hidalgo E, Demple B. Spacing of promoter elements regulates the basal expression of the soxS gene and converts SoxR from a transcriptional activator into a repressor. EMBO J 1997; 16: 1056\u20131065."},{"key":"B69","series-title":"Trends Biochem Sci","first-page":"207","article-title":"Redox signal transduction via iron-sulfur clusters in the SoxR transcription activator","volume":"22","author":"Hidalgo E","year":"1997","unstructured":"Hidalgo E, Ding H, Demple B. Redox signal transduction via iron-sulfur clusters in the SoxR transcription activator. Trends Biochem Sci 1997; 22: 207\u2013210."},{"key":"B70","series-title":"Microbiol Spectr","article-title":"Roles of SmeYZ, SbiAB, and SmeDEF efflux systems in iron homeostasis of Stenotrophomonas maltophilia","volume":"10","author":"Wu CJ","year":"2022","unstructured":"Wu CJ, Chen Y, Li LH, Wu CM, Lin YT, Ma CH, et\u00a0al. Roles of SmeYZ, SbiAB, and SmeDEF efflux systems in iron homeostasis of Stenotrophomonas maltophilia. Microbiol Spectr 2022; 10: e0244821."},{"key":"B71","series-title":"PLoS One","article-title":"Regulation by SoxR of mfsA, which encodes a major facilitator protein involved in paraquat resistance in Stenotrophomonas maltophilia","volume":"10","author":"Srijaruskul K","year":"2015","unstructured":"Srijaruskul K, Charoenlap N, Namchaiw P, Chattrakarn S, Giengkam S, Mongkolsuk S, et\u00a0al. Regulation by SoxR of mfsA, which encodes a major facilitator protein involved in paraquat resistance in Stenotrophomonas maltophilia. PLoS One 2015; 10: e0123699."},{"key":"B72","series-title":"J Antimicrob Chemother","first-page":"1263","article-title":"Overexpression of Stenotrophomonas maltophilia major facilitator superfamily protein MfsA increases resistance to fluoroquinolone antibiotics","volume":"73","author":"Vattanaviboon P","year":"2018","unstructured":"Vattanaviboon P, Dulyayangkul P, Mongkolsuk S, Charoenlap N. 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Expression of the soxR gene of Pseudomonas aeruginosa is inducible during infection of burn wounds in mice and is required to cause efficient bacteremia. Infect Immun 1999; 67: 5324\u20135331."},{"key":"B75","series-title":"Front Microbiol","article-title":"The fusaric acid derivative qy17 inhibits Staphylococcus haemolyticus by disrupting biofilm formation and the stress response via altered gene expression","volume":"13","author":"Wang B","year":"2022","unstructured":"Wang B, Song CR, Zhang QY, Wei PW, Wang X, Long YH, et\u00a0al. The fusaric acid derivative qy17 inhibits Staphylococcus haemolyticus by disrupting biofilm formation and the stress response via altered gene expression. Front Microbiol 2022; 13: 822148."},{"key":"B76","series-title":"Pharmacol Rep","first-page":"1","article-title":"Efflux pump inhibitors: new updates","volume":"73","author":"AlMatar M","year":"2021","unstructured":"AlMatar M, Albarri O, Makky EA, Koksal F. Efflux pump inhibitors: new updates. Pharmacol Rep 2021; 73: 1\u201316."},{"key":"B77","series-title":"Front Microbiol","article-title":"Function and inhibitory mechanisms of multidrug efflux pumps","volume":"12","author":"Nishino K","year":"2021","unstructured":"Nishino K, Yamasaki S, Nakashima R, Zwama M, Hayashi-Nishino M. Function and inhibitory mechanisms of multidrug efflux pumps. Front Microbiol 2021; 12: 737288."},{"key":"B78","series-title":"Plos Biol","article-title":"Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors","volume":"5","author":"Sennhauser G","year":"2007","unstructured":"Sennhauser G, Amstutz P, Briand C, Storchenegger O, Grutter MG. Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. Plos Biol 2007; 5: e7."},{"key":"B79","series-title":"Antibiotics (Basel)","article-title":"Update on the discovery of efflux pump inhibitors against critical priority Gram-negative bacteria","volume":"12","author":"Compagne N","year":"2023","unstructured":"Compagne N, Vieira Da Cruz A, Muller RT, Hartkoorn RC, Flipo M, Pos KM. Update on the discovery of efflux pump inhibitors against critical priority Gram-negative bacteria. Antibiotics (Basel) 2023; 12."},{"key":"B80","series-title":"Bioorg Med Chem Lett","first-page":"4201","article-title":"MexAB-OprM-specific efflux pump inhibitors in Pseudomonas aeruginosa. Part 1: discovery and early strategies for lead optimization","volume":"13","author":"Nakayama K","year":"2003","unstructured":"Nakayama K, Ishida Y, Ohtsuka M, Kawato H, Yoshida K, Yokomizo Y, et\u00a0al. MexAB-OprM-specific efflux pump inhibitors in Pseudomonas aeruginosa. Part 1: discovery and early strategies for lead optimization. Bioorg Med Chem Lett 2003; 13: 4201\u20134204."},{"key":"B81","series-title":"ACS Infect Dis","first-page":"1458","article-title":"Extending the potency and lifespan of antibiotics: inhibitors of Gram-negative bacterial efflux pumps","volume":"10","author":"Duffey M","year":"2024","unstructured":"Duffey M, Jumde RP, da Costa RMA, Ropponen HK, Blasco B, Piddock LJV. Extending the potency and lifespan of antibiotics: inhibitors of Gram-negative bacterial efflux pumps. ACS Infect Dis 2024; 10: 1458\u20131482."},{"key":"B82","series-title":"Antimicrob Agents Chemother","first-page":"3215","article-title":"Effects of efflux pump inhibitors on colistin resistance in multidrug-resistant gram-negative bacteria","volume":"60","author":"Ni W","year":"2016","unstructured":"Ni W, Li Y, Guan J, Zhao J, Cui J, Wang R, et\u00a0al. Effects of efflux pump inhibitors on colistin resistance in multidrug-resistant gram-negative bacteria. Antimicrob Agents Chemother 2016; 60: 3215\u20133218."},{"key":"B83","series-title":"Biology (Basel)","article-title":"Drug efflux pump inhibitors: a promising approach to counter multidrug resistance in gram-negative pathogens by targeting AcrB protein from AcrAB-TolC multidrug efflux pump from Escherichia coli","volume":"11","author":"Alenazy R","year":"2022","unstructured":"Alenazy R. Drug efflux pump inhibitors: a promising approach to counter multidrug resistance in gram-negative pathogens by targeting AcrB protein from AcrAB-TolC multidrug efflux pump from Escherichia coli. Biology (Basel) 2022; 11."},{"key":"B84","series-title":"Front Cell Infect Microbiol","first-page":"373","article-title":"Neutrophils to the ROScue: mechanisms of NADPH oxidase activation and bacterial resistance","volume":"7","author":"Nguyen GT","year":"2017","unstructured":"Nguyen GT, Green ER, Mecsas J. Neutrophils to the ROScue: mechanisms of NADPH oxidase activation and bacterial resistance. Front Cell Infect Microbiol 2017; 7: 373."},{"key":"B85","series-title":"Microb Drug Resist","first-page":"163","article-title":"Levofloxacin efflux and smeD in clinical isolates of Stenotrophomonas maltophilia","volume":"23","author":"Chong SY","year":"2017","unstructured":"Chong SY, Lee K, Chung HS, Hong SG, Suh Y, Chong Y. Levofloxacin efflux and smeD in clinical isolates of Stenotrophomonas maltophilia. Microb Drug Resist 2017; 23: 163\u2013168."},{"key":"B86","series-title":"Biology (Basel)","article-title":"The contribution of efflux systems to levofloxacin resistance in Stenotrophomonas maltophilia clinical strains isolated in Warsaw, Poland","volume":"11","author":"Zajac OM","year":"2022","unstructured":"Zajac OM, Tyski S, Laudy AE. The contribution of efflux systems to levofloxacin resistance in Stenotrophomonas maltophilia clinical strains isolated in Warsaw, Poland. Biology (Basel) 2022; 11."},{"key":"B87","series-title":"Curr Opin Infect Dis","first-page":"572","article-title":"Treatment approaches for severe Stenotrophomonas maltophilia infections","volume":"36","author":"Mojica MF","year":"2023","unstructured":"Mojica MF, Bonomo RA, van Duin D. Treatment approaches for severe Stenotrophomonas maltophilia infections. 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