Synergistic Effects of Baicalin and Levofloxacin Against Hypervirulent Klebsiella pneumoniae Biofilm In Vitro.
Journal
Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448
Informations de publication
Date de publication:
06 Mar 2023
06 Mar 2023
Historique:
received:
14
11
2022
accepted:
12
02
2023
entrez:
6
3
2023
pubmed:
7
3
2023
medline:
9
3
2023
Statut:
epublish
Résumé
Hypervirulent Klebsiella pneumoniae (hvKp) strains that form biofilms have recently emerged worldwide; however, the mechanisms underlying biofilm formation and disruption remain elusive. In this study, we established a hvKp biofilm model, investigated its in vitro formation pattern, and determined the mechanism of biofilm destruction by baicalin (BA) and levofloxacin (LEV). Our results revealed that hvKp exhibited a strong biofilm-forming ability, forming early and mature biofilms after 3 and 5 d, respectively. Early biofilm and bacterial burden were significantly reduced by BA + LEV and EM + LEV treatments, which destroyed the 3D structure of early biofilms. Conversely, these treatments were less effective against mature biofilm. The expression of both AcrA and wbbM was significantly downregulated in the BA + LEV group. These findings indicated that BA + LEV might inhibit the formation of hvKp biofilm by altering the expression of genes regulating efflux pumps and lipopolysaccharide biosynthesis.
Identifiants
pubmed: 36877407
doi: 10.1007/s00284-023-03226-y
pii: 10.1007/s00284-023-03226-y
doi:
Substances chimiques
baicalin
347Q89U4M5
Levofloxacin
6GNT3Y5LMF
Flavonoids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
126Subventions
Organisme : National Natural Science Foundation of China
ID : 82104499
Organisme : Guangxi Health Commission Key Lab of Fungi and Mycosis Research and Prevention
ID : ZZH2020004
Organisme : The First Affiliated Hospital of Guangxi Medical University Provincial and Ministerial Key Laboratory Cultivation Project: Guangxi Key Laboratory of Tropical Fungi and Mycosis Research
ID : YYZS2020006
Organisme : Guangxi Health Commission Self-financing Project
ID : Z20210909
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Wong Fok Lung T, Charytonowicz D, Beaumont KG et al (2022) Klebsiella pneumoniae induces host metabolic stress that promotes tolerance to pulmonary infection. Cell Metab 34:761-774.e9. https://doi.org/10.1016/j.cmet.2022.03.009
doi: 10.1016/j.cmet.2022.03.009
pubmed: 35413274
Wang G, Zhao G, Chao X, Xie L, Wang H (2020) The Characteristic of virulence, biofilm and antibiotic resistance of Klebsiella pneumoniae. Int J Environ Res Public Health 17:6278. https://doi.org/10.3390/ijerph17176278
doi: 10.3390/ijerph17176278
pubmed: 32872324
pmcid: 7503635
Zhang Y, Yao Z, Zhan S, Yang Z, Wei D, Zhang J, Li J, Kyaw MH (2014) Disease burden of intensive care unit-acquired pneumonia in China: a systematic review and meta-analysis. Int J Infect Dis 29:84–90. https://doi.org/10.1016/j.ijid.2014.05.030
doi: 10.1016/j.ijid.2014.05.030
pubmed: 25449241
Chew KL, Lin RTP, Teo JWP (2017) Klebsiella pneumoniae in Singapore: Hypervirulent Infections and the Carbapenemase Threat. Front Cell Infect Microbiol 7:515. https://doi.org/10.3389/fcimb.2017.00515
doi: 10.3389/fcimb.2017.00515
pubmed: 29312894
pmcid: 5732907
Russo TA, Olson R, Fang CT, Stoesser N, Miller M, MacDonald U, Hutson A, Barker JH, La Hoz RM, Johnson JR (2018) Identification of biomarkers for differentiation of hypervirulent Klebsiella pneumoniae from classical K. pneumoniae. J Clin Microbiol 56:e00776-e818. https://doi.org/10.1128/JCM.00776-18
doi: 10.1128/JCM.00776-18
pubmed: 29925642
pmcid: 6113484
Nassif X, Fournier JM, Arondel J, Sansonetti PJ (1989) Mucoid phenotype of Klebsiella pneumoniae is a plasmid-encoded virulence factor. Infect Immun 57:546–552. https://doi.org/10.1128/iai.57.2.546-552.1989
doi: 10.1128/iai.57.2.546-552.1989
pubmed: 2643575
pmcid: 313131
Liu Y, Cheng DL, Lin CL (1986) Klebsiella pneumoniae liver abscess associated with septic endophthalmitis. Arch Intern Med 146:1913–1916. https://doi.org/10.1001/archinte.1986.00360220057011
doi: 10.1001/archinte.1986.00360220057011
pubmed: 3532983
Russo TA, Marr CM (2019) Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev 32:e00001-19. https://doi.org/10.1128/CMR.00001-19
doi: 10.1128/CMR.00001-19
pubmed: 31092506
pmcid: 6589860
Edgar L, Pu T, Porter B, Aziz JM, La Pointe C, Asthana A, Orlando G (2020) Regenerative medicine, organ bioengineering and transplantation. Br J Surg 107:793–800. https://doi.org/10.1002/bjs.11686
doi: 10.1002/bjs.11686
pubmed: 32463143
Cometta S, Jones RT, Juárez-Saldivar A et al (2022) Melimine-modified 3D-printed polycaprolactone scaffolds for the prevention of biofilm-related biomaterial infections. ACS Nano 16:16497–16512. https://doi.org/10.1021/acsnano.2c05812
doi: 10.1021/acsnano.2c05812
pubmed: 36245096
pmcid: 9620410
Arciola CR, Campoccia D, Montanaro L (2018) Implant infections: adhesion, biofilm formation and immune evasion. Nat Rev Microbiol 16:397–409. https://doi.org/10.1038/s41579-018-0019-y
doi: 10.1038/s41579-018-0019-y
pubmed: 29720707
Hall CW, Mah TF (2017) Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev 41:276–301. https://doi.org/10.1093/femsre/fux010
doi: 10.1093/femsre/fux010
pubmed: 28369412
Jukič M, Bren U (2022) Machine learning in antibacterial drug design. Front Pharmacol 13:864412. https://doi.org/10.3389/fphar.2022.864412
doi: 10.3389/fphar.2022.864412
pubmed: 35592425
pmcid: 9110924
Arya SS, Sharma MM, Das RK, Rookes J, Cahill D, Lenka SK (2019) Heliyon 5:e02021. https://doi.org/10.1016/j.heliyon.2019.e02021
doi: 10.1016/j.heliyon.2019.e02021
pubmed: 31312733
pmcid: 6609825
Leung KC, Seneviratne CJ, Li X, Leung PC, Lau CB, Wong CH, Pang KY, Wong CW, Wat E, Jin L (2016) Synergistic antibacterial effects of nanoparticles encapsulated with Scutellaria baicalensis and pure chlorhexidine on oral bacterial biofilms. Nanomaterials 6:61. https://doi.org/10.3390/nano6040061
doi: 10.3390/nano6040061
pubmed: 28335189
pmcid: 5302556
Huang T, Liu Y, Zhang C (2019) Pharmacokinetics and bioavailability enhancement of baicalin: a review. Eur J Drug Metab Pharmacokinet 44:159–168. https://doi.org/10.1007/s13318-018-0509-3
doi: 10.1007/s13318-018-0509-3
pubmed: 30209794
Du Z, Huang Y, Chen Y, Chen Y (2019) Combination effects of baicalin with levofloxacin against biofilm-related infections. Am J Transl Res 11:1270–1281
pubmed: 30972161
pmcid: 6456525
Bush NG, Diez-Santos I, Abbott LR, Maxwell A (2020) Quinolones: mechanism, lethality and their contributions to antibiotic resistance. Molecules 25:5662. https://doi.org/10.3390/molecules25235662
doi: 10.3390/molecules25235662
pubmed: 33271787
pmcid: 7730664
Pu Y, Pan J, Yao Y, Ngan WY, Yang Y, Li M, Habimana O (2021) Ecotoxicological effects of erythromycin on a multispecies biofilm model, revealed by metagenomic and metabolomic approaches. Environ Pollut 276:116737. https://doi.org/10.1016/j.envpol.2021.116737
doi: 10.1016/j.envpol.2021.116737
pubmed: 33618119
Shendurnikar N (1988) Erythromycin. Indian Pediatr 25:780–783
pubmed: 3065241
Sayeed MA, Latif N, Mahmood SF (2017) Hypermucoviscous Klebsiella syndrome it’s in the community! J Pak Med Assoc 67:1930–1932
pubmed: 29256546
Vuotto C, Longo F, Pascolini C, Donelli G, Balice MP, Libori MF, Tiracchia V, Salvia A, Varaldo PE (2017) Biofilm formation and antibiotic resistance in Klebsiella pneumoniae urinary strains. J Appl Microbiol 123:1003–1018. https://doi.org/10.1111/jam.13533
doi: 10.1111/jam.13533
pubmed: 28731269
Chantell C, Humphries RM, Lewis II JS (2019) Clinical and laboratory standards institute, fluoroquinolone breakpoints for enterobacteriaceae and pseudomonas aeruginosa. CLSI Rationale: document MR02. CLSI, Wayne
Herigstad B, Hamilton M, Heersink J (2001) How to optimize the drop plate method for enumerating bacteria. J Microbiol Methods 44:121–129. https://doi.org/10.1016/s0167-7012(00)00241-4
doi: 10.1016/s0167-7012(00)00241-4
pubmed: 11165341
Coffey BM, Anderson GG (2014) Biofilm formation in the 96-well microtiter plate. Methods Mol Biol 1149:631–641. https://doi.org/10.1007/978-1-4939-0473-0_48
doi: 10.1007/978-1-4939-0473-0_48
pubmed: 24818938
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
doi: 10.1038/nprot.2008.73
pubmed: 18546601
Catalán-Nájera JC, Garza-Ramos U, Barrios-Camacho H (2017) Hypervirulence and hypermucoviscosity: Two different but complementary Klebsiella spp. phenotypes? Virulence 8:1111–1123. https://doi.org/10.1080/21505594.2017.1317412
doi: 10.1080/21505594.2017.1317412
pubmed: 28402698
pmcid: 5711391
Zhang Y, Zhao C, Wang Q, Wang X, Chen H, Li H, Zhang F, Li S, Wang R, Wang H (2016) High prevalence of hypervirulent Klebsiella pneumoniae infection in China: geographic distribution, clinical characteristics, and antimicrobial resistance. Antimicrob Agents Chemother 60:6115–6120. https://doi.org/10.1128/AAC.01127-16
doi: 10.1128/AAC.01127-16
pubmed: 27480857
pmcid: 5038323
Yang Y, Liu JH, Hu XX, Zhang W, Nie TY, Yang XY, Wang XK, Li CR, You XF (2020) Clinical and microbiological characteristics of hypervirulent Klebsiella pneumoniae (hvKp) in a hospital from North China. J Infect Dev Ctries 14:606–613. https://doi.org/10.3855/jidc.12288
doi: 10.3855/jidc.12288
pubmed: 32683351
Ling N, Forsythe S, Wu Q, Ding Y, Zhang J, Zeng H (2020) Insights into Cronobacter sakazakii biofilm formation and control strategies in the food industry. Engineering 6:393–405. https://doi.org/10.1016/j.eng.2020.02.007
doi: 10.1016/j.eng.2020.02.007
Singla S, Harjai K, Chhibber S (2014) Artificial Klebsiella pneumoniae biofilm model mimicking in vivo system: altered morphological characteristics and antibiotic resistance. J Antibiot 67:305–309. https://doi.org/10.1038/ja.2013.139
doi: 10.1038/ja.2013.139
Xu Z, Liu F, Wang X (2001) Effects of erythromycin and fosfomycin on pseudomonas aeruginosa biofilm in vitro. Zhonghua Jie He Hu Xi Za Zhi 24:342–344
Guan Y, Li C, Shi JJ, Zhou HN, Liu L, Wang Y, Pu YP (2013) Effect of combination of sub-MIC sodium houttuyfonate and erythromycin on biofilm of staphylococcus epidermidis. Zhongguo Zhong Yao Za Zhi 38:731–735
pubmed: 23724685
Müller RT, Pos KM (2015) The assembly and disassembly of the AcrAB-TolC three-component multidrug efflux pump. Biol Chem 396:1083–1089. https://doi.org/10.1515/hsz-2015-0150
doi: 10.1515/hsz-2015-0150
pubmed: 26061621
Heacock-Kang Y, Sun Z, Zarzycki-Siek J, Poonsuk K, McMillan IA, Chuanchuen R, Hoang TT (2018) Two regulators, PA3898 and PA2100, modulate the pseudomonas aeruginosa multidrug resistance MexAB-OprM and EmrAB efflux pumps and biofilm formation. Antimicrob Agents Chemother 62:e01459-e1518. https://doi.org/10.1128/AAC.01459-18
doi: 10.1128/AAC.01459-18
pubmed: 30297364
pmcid: 6256797
Ugwuanyi FC, Ajayi A, Ojo DA, Adeleye AI, Smith SI (2021) Evaluation of efflux pump activity and biofilm formation in multidrug resistant clinical isolates of Pseudomonas aeruginosa isolated from a Federal Medical Center in Nigeria. Ann Clin Microbiol Antimicrob 20:11. https://doi.org/10.1186/s12941-021-00417-y
doi: 10.1186/s12941-021-00417-y
pubmed: 33531042
pmcid: 7852189
Tang M, Wei X, Wan X, Ding Z, Ding Y, Liu J (2020) The role and relationship with efflux pump of biofilm formation in Klebsiella pneumoniae. Microb Pathog 147:104244. https://doi.org/10.1016/j.micpath.2020.104244
doi: 10.1016/j.micpath.2020.104244
pubmed: 32437832
Langstraat J, Bohse M, Clegg S (2001) Type 3 fimbrial shaft (MrkA) of Klebsiella pneumoniae, but not the fimbrial adhesin (MrkD), facilitates biofilm formation. Infect Immun 69:5805–5812. https://doi.org/10.1128/IAI.69.9.5805-5812.2001
doi: 10.1128/IAI.69.9.5805-5812.2001
pubmed: 11500458
pmcid: 98698
Alkhudhairy MK, Alshadeedi SMJ, Mahmood SS, Al-Bustan SA, Ghasemian A (2019) Comparison of adhesin genes expression among Klebsiella oxytoca ESBL-non-producers in planktonic and biofilm mode of growth, and imipenem sublethal exposure. Microb Pathog 134:103558. https://doi.org/10.1016/j.micpath.2019.103558
doi: 10.1016/j.micpath.2019.103558
pubmed: 31136790
Bakhtiari R, Javadi A, Aminzadeh M, Molaee-Aghaee E, Shaffaghat Z (2021) Association between presence of RmpA, MrkA and MrkD genes and antibiotic resistance in clinical Klebsiella pneumoniae isolates from hospitals in Tehran. Iran. Iran J Public Health 50:1009–1016. https://doi.org/10.18502/ijph.v50i5.6118
doi: 10.18502/ijph.v50i5.6118
pubmed: 34183959
Maldonado RF, Sá-Correia I, Valvano MA (2016) Lipopolysaccharide modification in Gram-negative bacteria during chronic infection. FEMS Microbiol Rev 40:480–493. https://doi.org/10.1093/femsre/fuw007
doi: 10.1093/femsre/fuw007
pubmed: 27075488
pmcid: 4931227
Wasfi R, Hamed SM, Amer MA, Fahmy LI (2020) Proteus mirabilis biofilm: development and therapeutic strategies. Front Cell Infect Microbiol 10:414. https://doi.org/10.3389/fcimb.2020.00414
doi: 10.3389/fcimb.2020.00414
pubmed: 32923408
pmcid: 7456845
Kos V, Whitfield C (2010) A membrane-located glycosyltransferase complex required for biosynthesis of the D-galactan I lipopolysaccharide O antigen in Klebsiella pneumoniae. J Biol Chem 285:19668–19687. https://doi.org/10.1074/jbc.M110.122598
doi: 10.1074/jbc.M110.122598
pubmed: 20410291
pmcid: 2885245
Clarke BR, Ovchinnikova OG, Sweeney RP, Kamski-Hennekam ER, Gitalis R, Mallette E, Kelly SD, Lowary TL, Kimber MS, Whitfield C (2020) A bifunctional O-antigen polymerase structure reveals a new glycosyltransferase family. Nat Chem Biol 16:450–457. https://doi.org/10.1038/s41589-020-0494-0
doi: 10.1038/s41589-020-0494-0
pubmed: 32152541
Chetri S, Bhowmik D, Dhar D, Chakravarty A, Bhattacharjee A (2019) Effect of concentration gradient carbapenem exposure on expression of blaNDM-1 and acrA in carbapenem resistant Escherichia coli. Infect Genet Evol 73:332–336. https://doi.org/10.1016/j.meegid.2019.05.024
doi: 10.1016/j.meegid.2019.05.024
pubmed: 31170528
Huang YQ, Huang GR, Wu MH et al (2015) Inhibitory effects of emodin, baicalin, schizandrin and berberine on hefA gene: treatment of Helicobacter pylori-induced multidrug resistance. World J Gastroenterol 21:4225–4231. https://doi.org/10.3748/wjg.v21.i14.4225
doi: 10.3748/wjg.v21.i14.4225
pubmed: 25892872
pmcid: 4394083
Wang J, Jiao H, Meng J, Qiao M, Du H, He M, Ming K, Liu J, Wang D, Wu Y (2019) Baicalin inhibits biofilm formation and the quorum-sensing system by regulating the MsrA drug efflux pump in Staphylococcus saprophyticus. Front Microbiol 10:2800. https://doi.org/10.3389/fmicb.2019.02800
doi: 10.3389/fmicb.2019.02800
pubmed: 31921008
pmcid: 6915091