Repurposing promethazine hydrochloride to inhibit biofilm formation against Burkholderia thailandensis.
Biofilms
/ drug effects
Burkholderia
/ drug effects
Promethazine
/ pharmacology
Drug Repositioning
Molecular Docking Simulation
Anti-Bacterial Agents
/ pharmacology
Lipase
/ metabolism
Gene Expression Regulation, Bacterial
/ drug effects
Bacterial Proteins
/ genetics
Humans
Quorum Sensing
/ drug effects
Burkholderia thailandensis
Biofilms
Drug repurposing
Lipase
Promethazine hydrochloride
Quorum sensing
Journal
Medical microbiology and immunology
ISSN: 1432-1831
Titre abrégé: Med Microbiol Immunol
Pays: Germany
ID NLM: 0314524
Informations de publication
Date de publication:
20 Jul 2024
20 Jul 2024
Historique:
received:
05
12
2023
accepted:
12
07
2024
medline:
21
7
2024
pubmed:
21
7
2024
entrez:
20
7
2024
Statut:
epublish
Résumé
Melioidosis is a severe infectious disease caused by Burkholderia pseudomallei, an intracellular pathogen with a high mortality rate and significant antibiotic resistance. The high mortality rate and resistance to antibiotics have drawn considerable attention from researchers studying melioidosis. This study evaluated the effects of various concentrations (75, 50, and 25 µg/mL) of promethazine hydrochloride (PTZ), a potent antihistamine, on biofilm formation and lipase activity after 24 h of exposure to B. thailandensis E264. A concentration-dependent decrease in both biofilm biomass and lipase activity was observed. RT-PCR analysis revealed that PTZ treatment not only made the biofilm structure loose but also reduced the expression of btaR1, btaR2, btaR3, and scmR. Single gene knockouts of quorum sensing (QS) receptor proteins (∆btaR1, ∆btaR2, and ∆btaR3) were successfully constructed. Deletion of btaR1 affected biofilm formation in B. thailandensis, while deletion of btaR2 and btaR3 led to reduced lipase activity. Molecular docking and biological performance results demonstrated that PTZ inhibits biofilm formation and lipase activity by suppressing the expression of QS-regulated genes. This study found that repositioning PTZ reduced biofilm formation in B. thailandensis E264, suggesting a potential new approach for combating melioidosis.
Identifiants
pubmed: 39033094
doi: 10.1007/s00430-024-00799-8
pii: 10.1007/s00430-024-00799-8
doi:
Substances chimiques
Promethazine
FF28EJQ494
Anti-Bacterial Agents
0
Lipase
EC 3.1.1.3
Bacterial Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
16Subventions
Organisme : Innovative Research Projects for Postgraduates in Hainan Province
ID : Qhyb2022-46
Organisme : Innovative Research Projects for Postgraduates in Hainan Province
ID : Qhyb2021-38
Organisme : National Natural Science Foundation of China
ID : 82160664
Organisme : Natural Science Foundation of Hainan Province
ID : 221CXTD434
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Mariappan V, Vellasamy KM, Barathan M, Girija ASS, Shankar EM, Vadivelu J (2021) Hijacking of the host’s immune surveillance radars by Burkholderia pseudomallei. Front Immunol 12:718719. https://doi.org/10.3389/fimmu.2021.718719
doi: 10.3389/fimmu.2021.718719
pubmed: 34456925
pmcid: 8384953
Currie BJ, Meumann EM, Kaestli M (2023) The expanding global footprint of Burkholderia pseudomallei and melioidosis. Am J Trop Med Hyg 108(6):1081–1083. https://doi.org/10.4269/ajtmh.23-0223
doi: 10.4269/ajtmh.23-0223
pubmed: 37160279
pmcid: 10540122
Bzdyl NM, Moran CL, Bendo J, Sarkar-Tyson M (2022) Pathogenicity and virulence of Burkholderia pseudomallei. Virulence 13(1):1945–1965. https://doi.org/10.1080/21505594.2022.2139063
doi: 10.1080/21505594.2022.2139063
pubmed: 36271712
pmcid: 9635556
Currie BJ (2022) Melioidosis and Burkholderia pseudomallei: progress in epidemiology, diagnosis, treatment and vaccination. Curr Opin Infect Dis 35(6):517–523. https://doi.org/10.1097/qco.0000000000000869
doi: 10.1097/qco.0000000000000869
pubmed: 35942848
Limmathurotsakul D, Golding N, Dance DA, Messina JP, Pigott DM, Moyes CL et al (2016) Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nat Microbiol 1:15008. https://doi.org/10.1038/nmicrobiol.2015.8
doi: 10.1038/nmicrobiol.2015.8
pubmed: 27571754
pmcid: 4746747
Greenberg EP, Chandler JR, Seyedsayamdost MR (2020) The chemistry and biology of Bactobolin: a 10-year collaboration with natural product chemist Extraordinaire Jon Clardy. J Nat Prod 83(3):738–743. https://doi.org/10.1021/acs.jnatprod.9b01237
doi: 10.1021/acs.jnatprod.9b01237
pubmed: 32105069
pmcid: 8118907
Godoy D, Randle G, Simpson AJ, Aanensen DM, Pitt TL, Kinoshita R et al (2003) Multilocus sequence typing and evolutionary relationships among the causative agents of melioidosis and glanders, Burkholderia pseudomallei and Burkholderia mallei. J Clin Microbiol 41(5):2068–2079. https://doi.org/10.1128/jcm.41.5.2068-2079.2003
doi: 10.1128/jcm.41.5.2068-2079.2003
pubmed: 12734250
pmcid: 154742
Correia J, Gudiña EJ, Lazar Z, Janek T, Teixeira JA (2022) Cost-effective rhamnolipid production by Burkholderia thailandensis E264 using agro-industrial residues. Appl Microbiol Biotechnol 106(22):7477–7489. https://doi.org/10.1007/s00253-022-12225-1
doi: 10.1007/s00253-022-12225-1
pubmed: 36222896
Franco M, D’Haeseleer PM, Branda SS, Liou MJ, Haider Y, Segelke BW et al (2018) Proteomic profiling of Burkholderia thailandensis during host infection using bio-orthogonal noncanonical amino acid tagging (BONCAT). Front Cell Infect Microbiol 8:370. https://doi.org/10.3389/fcimb.2018.00370
doi: 10.3389/fcimb.2018.00370
pubmed: 30406044
pmcid: 6206043
Sauer K, Stoodley P, Goeres DM, Hall-Stoodley L, Burmølle M, Stewart PS et al (2022) The biofilm life cycle: expanding the conceptual model of biofilm formation. Nat Rev Microbiol 20(10):608–620. https://doi.org/10.1038/s41579-022-00767-0
doi: 10.1038/s41579-022-00767-0
pubmed: 35922483
pmcid: 9841534
Wongkaewkhiaw S, Taweechaisupapong S, Anutrakunchai C, Nazmi K, Bolscher JGM, Wongratanacheewin S et al (2019) D-LL-31 in combination with ceftazidime synergistically enhances bactericidal activity and biofilm destruction in Burkholderia pseudomallei. Biofouling 35(5):573–584. https://doi.org/10.1080/08927014.2019.1632835
doi: 10.1080/08927014.2019.1632835
pubmed: 31282211
Tseng BS, Majerczyk CD, Passos da Silva D, Chandler JR, Greenberg EP, Parsek MR (2016) Quorum sensing influences Burkholderia thailandensis biofilm development and matrix production. J Bacteriol 198(19):2643–2650. https://doi.org/10.1128/JB.00047-16
doi: 10.1128/JB.00047-16
pubmed: 27068594
pmcid: 5019063
Prazdnova EV, Gorovtsov AV, Vasilchenko NG, Kulikov MP, Statsenko VN, Bogdanova AA et al (2022) Quorum-sensing inhibition by gram-positive bacteria. Microorganisms 10(2):350. https://doi.org/10.3390/microorganisms10020350
doi: 10.3390/microorganisms10020350
pubmed: 35208805
pmcid: 8875677
Ulrich RL, Hines HB, Parthasarathy N, Jeddeloh JA (2004) Mutational analysis and biochemical characterization of the Burkholderia thailandensis DW503 quorum-sensing network. J Bacteriol 186(13):4350–4360. https://doi.org/10.1128/JB.186.13.4350-4360.2004
doi: 10.1128/JB.186.13.4350-4360.2004
pubmed: 15205437
pmcid: 421622
Duerkop BA, Varga J, Chandler JR, Peterson SB, Herman JP, Churchill ME et al (2009) Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis. J Bacteriol 191(12):3909–3918. https://doi.org/10.1128/jb.00200-09
doi: 10.1128/jb.00200-09
pubmed: 19376863
pmcid: 2698390
Le Guillouzer S, Groleau MC, Deziel E (2017) The complex quorum sensing circuitry of Burkholderia thailandensis Ss both hierarchically and homeostatically organized. mBio 8(6):e01861–e01817. https://doi.org/10.1128/mBio.01861-17
doi: 10.1128/mBio.01861-17
pubmed: 29208745
pmcid: 5717390
Hegazy WAH, Khayat MT, Ibrahim TS, Nassar MS, Bakhrebah MA, Abdulaal WH et al (2020) Repurposing anti-diabetic drugs to cripple quorum sensing in Pseudomonas aeruginosa. Microorganisms 8(9):1285. https://doi.org/10.3390/microorganisms8091285
doi: 10.3390/microorganisms8091285
pubmed: 32842696
pmcid: 7569791
Morales D, Micheva-Viteva S, Adikari S, Werner J, Wolinsky M, Hong-Geller E et al (2022) Targeting the bet-hedging strategy with an inhibitor of bacterial efflux capacity enhances antibiotic efficiency and ameliorates bacterial persistence in vitro. Microorganisms 10(10):1966
doi: 10.3390/microorganisms10101966
pubmed: 36296242
pmcid: 9609472
Xu K-Z, Xiang S-L, Wang Y-J, Wang B, Jia A-Q (2023) Methyl gallate isolated from partridge tea (Mallotus Oblongifolius (Miq.) Müll.Arg.) Inhibits the biofilms and virulence factors of Burkholderia thailandensis. J Ethnopharmacol 320:117422. https://doi.org/10.1016/j.jep.2023.117422
doi: 10.1016/j.jep.2023.117422
pubmed: 37977424
Memariani H, Memariani M (2023) Antibiofilm properties of cathelicidin LL-37: an in-depth review. World J Microbiol Biotechnol 39(4):99. https://doi.org/10.1007/s11274-023-03545-z
doi: 10.1007/s11274-023-03545-z
pubmed: 36781570
Glenn AW, Roberto FF, Ward TE (1992) Transformation of acidiphilium by electroporation and conjugation. Can J Microbiol 38(5):387–393. https://doi.org/10.1139/m92-065
doi: 10.1139/m92-065
pubmed: 1643582
Yin L, Zhang PP, Wang W, Tang S, Deng SM, Jia AQ (2022) 3-Phenylpropan-1-amine enhanced susceptibility of Serratia marcescens to ofloxacin by occluding quorum sensing. Microbiol Spectr 10(5):e0182922. https://doi.org/10.1128/spectrum.01829-22
doi: 10.1128/spectrum.01829-22
pubmed: 35972277
Zhou JW, Ruan LY, Chen HJ, Luo HZ, Jiang H, Wang JS et al (2019) Inhibition of quorum sensing and virulence in Serratia marcescens by hordenine. J Agric Food Chem 67(3):784–795. https://doi.org/10.1021/acs.jafc.8b05922
doi: 10.1021/acs.jafc.8b05922
pubmed: 30609368
Xu KZ, Tan XJ, Chang ZY, Li JJ, Jia AQ (2022) 2-tert-Butyl-1,4-benzoquinone, a food additive oxidant, reduces virulence factors of Chromobacterium violaceum. LWT-Food Sci Technol 163:113569. https://doi.org/10.1016/j.lwt.2022.113569
doi: 10.1016/j.lwt.2022.113569
Paytubi S, Guirado P, Balsalobre C, Madrid C (2014) An improved and versatile methodology to quantify biofilms formed on solid surfaces and exposed to the air-liquid interphase. J Microbiol Methods 103:77–79. https://doi.org/10.1016/j.mimet.2014.05.020
doi: 10.1016/j.mimet.2014.05.020
pubmed: 24892512
Uchil PD, Nagarajan A, Kumar P (2017) β-Galactosidase. Cold Spring Harb Protoc 2017(10):774–779. https://doi.org/10.1101/pdb.top096198
doi: 10.1101/pdb.top096198
Zhang X, Bremer H (1995) Control of the Escherichia coli rrnB P1 promoter strength by ppGpp. J Biol Chem 270(19):11181–11189. https://doi.org/10.1074/jbc.270.19.11181
doi: 10.1074/jbc.270.19.11181
pubmed: 7538113
David C, Heuschkel I, Buhler K, Karande R (2020) Cultivation of productive biofilms in flow reactors and their characterization by CLSM. Methods in molecular biology. (Clifton N J) 2100:437–452. https://doi.org/10.1007/978-1-0716-0215-7_30
doi: 10.1007/978-1-0716-0215-7_30
Li X, Liu Y, Wang Y, Lin Z, Wang D, Sun H (2021) Resistance risk induced by quorum sensing inhibitors and their combined use with antibiotics: mechanism and its relationship with toxicity. Chemosphere 265:129153. https://doi.org/10.1016/j.chemosphere.2020.129153
doi: 10.1016/j.chemosphere.2020.129153
pubmed: 33302207
Gupta A, Fuentes SM, Grove A (2017) Redox-sensitive MarR homologue BifR from Burkholderia thailandensis regulates biofilm formation. Biochemistry 56(17):2315–2327. https://doi.org/10.1021/acs.biochem.7b00103
doi: 10.1021/acs.biochem.7b00103
pubmed: 28406615
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Seeliger D, de Groot BL (2010) Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J Comput Aided Mol Des 24(5):417–422. https://doi.org/10.1007/s10822-010-9352-6
doi: 10.1007/s10822-010-9352-6
pubmed: 20401516
pmcid: 2881210
Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G et al (2022) AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res 50(D1):D439–d444. https://doi.org/10.1093/nar/gkab1061
doi: 10.1093/nar/gkab1061
pubmed: 34791371
Abbas HA, Hegazy WAH (2020) Repurposing anti-diabetic drug sitagliptin as a novel virulence attenuating agent in Serratia marcescens. PLoS ONE 15(4):e0231625. https://doi.org/10.1371/journal.pone.0231625
doi: 10.1371/journal.pone.0231625
pubmed: 32298346
pmcid: 7162429
Pant N, Miranda-Hernandez S, Rush C, Warner J, Eisen DP (2022) Non-antimicrobial adjuvant therapy using ticagrelor reduced biofilm-related Staphylococcus aureus prosthetic ioint infection. Front Pharmacol 13:927783. https://doi.org/10.3389/fphar.2022.927783
doi: 10.3389/fphar.2022.927783
pubmed: 35846990
pmcid: 9284533
Sakaguchi T, Ohkawara B, Kishimoto Y, Miyamoto K, Ishizuka S, Hiraiwa H et al (2022) Promethazine downregulates wnt/β-catenin signaling and increases the biomechanical forces of the injured achilles tendon in the early stage of healing. Am J Sports Med 50(5):1317–1327. https://doi.org/10.1177/03635465221077116
doi: 10.1177/03635465221077116
pubmed: 35234523
Ghiasi Z, Validad MH, Ostadkelayeh SM, Mazloom S, Avval JO, Moshari M et al (2022) Promethazine hydrochloride reduces children’s agitation during ocular examination for trauma. Eur J Transl Myol. https://doi.org/10.4081/ejtm.2022.10808
doi: 10.4081/ejtm.2022.10808
pubmed: 36073862
pmcid: 10141751
Donnert M, Elsheikh S, Arce-Rodriguez A, Pawar V, Braubach P, Jonigk D et al (2020) Targeting bioenergetics is key to counteracting the drug-tolerant state of biofilm-grown bacteria. PLoS Pathog 16(12):e1009126. https://doi.org/10.1371/journal.ppat.1009126
doi: 10.1371/journal.ppat.1009126
pubmed: 33351859
pmcid: 7787680
Anutrakunchai C, Bolscher JGM, Krom BP, Kanthawong S, Chareonsudjai S, Taweechaisupapong S (2018) Impact of nutritional stress on drug susceptibility and biofilm structures of Burkholderia pseudomallei and Burkholderia thailandensis grown in static and microfluidic systems. PLoS ONE 13(3):e0194946. https://doi.org/10.1371/journal.pone.0194946
doi: 10.1371/journal.pone.0194946
pubmed: 29579106
pmcid: 5868842
Hu C, Xiong N, Zhang Y, Rayner S, Chen S (2012) Functional characterization of lipase in the pathogenesis of Staphylococcus aureus. Biochem Biophys Res Commun 419(4):617–620. https://doi.org/10.1016/j.bbrc.2012.02.057
doi: 10.1016/j.bbrc.2012.02.057
pubmed: 22369949
Mullen T, Markey K, Murphy P, McClean S, Callaghan M (2007) Role of lipase in Burkholderia cepacia complex (bcc) invasion of lung epithelial cells. Eur J Clin Microbiol Infect Dis 26(12):869–877. https://doi.org/10.1007/s10096-007-0385-2
doi: 10.1007/s10096-007-0385-2
pubmed: 17874328
Irudal S, Scoffone VC, Trespidi G, Barbieri G, D’Amato M, Viglio S et al (2023) Identification by reverse vaccinology of three virulence factors in Burkholderia cenocepacia that may represent ideal vaccine antigens. Vaccines 11(6):1039. https://doi.org/10.3390/vaccines11061039
doi: 10.3390/vaccines11061039
pubmed: 37376428
pmcid: 10303873
Kanekar S, Fathima F, Rekha PD (2022) Carvone - a quorum sensing inhibitor blocks biofilm formation in Chromobacterium violaceum. Nat Prod Res 36(17):4546–4551. https://doi.org/10.1080/14786419.2021.1993214
doi: 10.1080/14786419.2021.1993214
pubmed: 34672225
Rather MA, Saha D, Bhuyan S, Jha AN, Mandal M (2022) Quorum quenching: a drug discovery approach against Pseudomonas aeruginosa. Microbiol Res 264:127173. https://doi.org/10.1016/j.micres.2022.127173
doi: 10.1016/j.micres.2022.127173
pubmed: 36037563
Mao D, Bushin LB, Moon K, Wu Y, Seyedsayamdost MR (2017) Discovery of scmR as a global regulator of secondary metabolism and virulence in Burkholderia thailandensis E264. Proc Natl Acad Sci U S A 114(14):E2920–e2928. https://doi.org/10.1073/pnas.1619529114
doi: 10.1073/pnas.1619529114
pubmed: 28320949
pmcid: 5389298
Le Guillouzer S, Groleau M-C, Mauffrey F, Déziel E (2020) ScmR, a global regulator of gene expression, quorum sensing, pH homeostasis, and virulence in burkholderia thailandensis. J Bacteriol 202(13). https://doi.org/10.1128/jb.00776-19