Biochanin A as an α-hemolysin inhibitor for combating methicillin-resistant Staphylococcus aureus infection.


Journal

World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472

Informations de publication

Date de publication:
27 Nov 2021
Historique:
received: 09 09 2021
accepted: 28 10 2021
entrez: 27 11 2021
pubmed: 28 11 2021
medline: 5 1 2022
Statut: epublish

Résumé

Methicillin-resistant Staphylococcus aureus (MRSA) is a multidrug-resistant pathogen that poses a significant risk to global health today. In S. aureus, α-hemolysin is an important virulence factor as it contributes to the capacity of the bacteria to infect the host. Here, we showed that biochanin A (bioA), an isoflavone present in red clover, cabbage and alfalfa, effectively inhibited hemolytic activity at a dose as low as 32 μg/mL. Further, western blot and RT-qPCR data showed that bioA reduced the production and expression of MRSA hemolysin in a dose-dependent manner. In addition, when different concentrations of bioA were added to a coculture system of A549 cells and S. aureus, it could significantly decrease cell injury. Importantly, the in vivo study showed that bioA could protect mice from pneumonia caused by a lethal dose of MRSA, as evidenced by improving their survival and reducing the number of bacterial colonies in lung tissues, the secretion of hemolysin into alveolar lavage fluid and the degree of pulmonary edema. In conclusion, biochanin A protected the host from MRSA infection by inhibiting the expression of the hemolysin of MRSA, which may provide experimental evidence for its development to a potential anti-MRSA drug.

Identifiants

pubmed: 34837116
doi: 10.1007/s11274-021-03182-4
pii: 10.1007/s11274-021-03182-4
doi:

Substances chimiques

Anti-Bacterial Agents 0
Bacterial Proteins 0
Hemolysin Proteins 0
Genistein DH2M523P0H
biochanin A U13J6U390T

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

6

Subventions

Organisme : Xinglin Scholar Project" of Changchun University of Chinese Medicine
ID : 2019
Organisme : Science and Technology Development Plan Project (2019) of Jilin Province Science and Technology Department
ID : 20190103080JH
Organisme : "Thirteenth Five-Year Plan" of Science and Technology Project of Education Department of Jilin Province
ID : No. JJKH20200906KJ

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Bernheimer AW, Schwartz LL (1963) Isolation and composition of staphylococcal alpha toxin. J Gen Microbiol 30:455–468. https://doi.org/10.1099/00221287-30-3-455
doi: 10.1099/00221287-30-3-455 pubmed: 13967637
Berube BJ, Bubeck Wardenburg J (2013) Staphylococcus aureus α-toxin: nearly a century of intrigue. Toxins 5(6):1140–1166. https://doi.org/10.3390/toxins5061140
doi: 10.3390/toxins5061140 pubmed: 23888516 pmcid: 3717774
Bhakdi S, Muhly M, Füssle R (1984) Correlation between toxin binding and hemolytic activity in membrane damage by staphylococcal alpha-toxin. Infect Immun 46(2):318–323. https://doi.org/10.1128/iai.46.2.318-323.1984
doi: 10.1128/iai.46.2.318-323.1984 pubmed: 6500692 pmcid: 261533
Brown EL, Dumitrescu O, Thomas D, Badiou C, Koers EM, Choudhury P, Vazquez V, Etienne J, Lina G, Vandenesch F, Bowden MG (2009) The Panton-Valentine leukocidin vaccine protects mice against lung and skin infections caused by Staphylococcus aureus USA300. Clin Microbiol Infect 15(2):156–164. https://doi.org/10.1111/j.1469-0691.2008.02648.x
doi: 10.1111/j.1469-0691.2008.02648.x pubmed: 19281461 pmcid: 2916703
Bubeck Wardenburg J, Patel RJ, Schneewind O (2007) Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect Immun 75(2):1040–1044. https://doi.org/10.1128/iai.01313-06
doi: 10.1128/iai.01313-06 pubmed: 17101657
Casadevall A, Pirofski LA (1999) Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun 67(8):3703–3713. https://doi.org/10.1128/iai.67.8.3703-3713.1999
doi: 10.1128/iai.67.8.3703-3713.1999 pubmed: 10417127 pmcid: 96643
Dan Z, Xie K, Wang H, Chen Y, Xie MJAMS (2014) Inhibitory effects of biochanin A on the efflux pump of methicillin-resistant Staphylococcus aureus (MRSA). Mol Med Rep 54(10):1204–1211
Derangula M, Panati K, Narala VR (2020) Biochanin A ameliorates ovalbumin-induced airway inflammation through peroxisome proliferator-activated receptor-gamma in a mouse model. EMIDDT 21:145
doi: 10.2174/1871530320666200503051609
Dickey SW, Cheung GYC, Otto M (2017) Different drugs for bad bugs: antivirulence strategies in the age of antibiotic resistance. Nat Rev Drug Discov 16(7):457–471. https://doi.org/10.1038/nrd.2017.23
doi: 10.1038/nrd.2017.23 pubmed: 28337021
Diep BA, Le VTM, Visram ZC, Rouha H, Stulik L, Dip EC, Nagy G, Nagy E (2016) Improved protection in a rabbit model of community-associated methicillin-resistant Staphylococcus aureus necrotizing pneumonia upon neutralization of leukocidins in addition to alpha-hemolysin. Antimicrob Agents Chemother 60:6333
doi: 10.1128/AAC.01213-16
Dinges MM, Orwin PM, Schlievert PM (2000) Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13(1):16–34. https://doi.org/10.1128/cmr.13.1.16
doi: 10.1128/cmr.13.1.16 pubmed: 10627489 pmcid: 88931
Dong J, Qiu J, Zhang Y, Lu C, Dai X, Wang J, Li H, Wang X, Tan W, Luo M, Niu X, Deng X (2013) Oroxylin A inhibits hemolysis via hindering the self-assembly of α-hemolysin heptameric transmembrane pore. PLoS Comput Biol 9(1):e1002869. https://doi.org/10.1371/journal.pcbi.1002869
doi: 10.1371/journal.pcbi.1002869 pubmed: 23349625 pmcid: 3547825
Fridman O, Goldberg A, Ronin I, Shoresh N, Balaban NQ (2014) Optimization of lag time underlies antibiotic tolerance in evolved bacterial populations. Nature 513(7518):418–421. https://doi.org/10.1038/nature13469
doi: 10.1038/nature13469 pubmed: 25043002
Fritz SA, Tiemann KM, Hogan PG, Epplin EK, Rodriguez M, Al-Zubeidi DN, Bubeck Wardenburg J, Hunstad DA (2013) A serologic correlate of protective immunity against community-onset Staphylococcus aureus infection. Clin Infect Dis 56(11):1554–1561. https://doi.org/10.1093/cid/cit123
doi: 10.1093/cid/cit123 pubmed: 23446627 pmcid: 3641868
Grumann D, Nübel U, Bröker BM (2014) Staphylococcus aureus toxins–their functions and genetics. Infect Genet Evol 21:583–592. https://doi.org/10.1016/j.meegid.2013.03.013
doi: 10.1016/j.meegid.2013.03.013 pubmed: 23541411
Jain A, Lai JC, Bhushan A (2015) Biochanin A inhibits endothelial cell functions and proangiogenic pathways: implications in glioma therapy. Anticancer Drugs 26(3):323–330. https://doi.org/10.1097/cad.0000000000000189
doi: 10.1097/cad.0000000000000189 pubmed: 25501542
Jiang L, Li H, Wang L, Song Z, Shi L, Li W, Deng X, Wang J (2016) Isorhamnetin attenuates Staphylococcus aureus-induced lung cell injury by inhibiting alpha-hemolysin expression. J Microbiol Biotechnol 26(3):596–602. https://doi.org/10.4014/jmb.1507.07091
doi: 10.4014/jmb.1507.07091 pubmed: 26643966
Kolata J, Bode LG, Holtfreter S, Steil L, Kusch H, Holtfreter B, Albrecht D, Hecker M, Engelmann S, van Belkum A, Völker U, Bröker BM (2011) Distinctive patterns in the human antibody response to Staphylococcus aureus bacteremia in carriers and non-carriers. Proteomics 11(19):3914–3927. https://doi.org/10.1002/pmic.201000760
doi: 10.1002/pmic.201000760 pubmed: 21805632
Kole L, Giri B, Manna SK, Pal B, Ghosh SJEJP (2011) Biochanin-A, an isoflavon, showed anti-proliferative and anti-inflammatory activities through the inhibition of iNOS expression, p38-MAPK and ATF-2 phosphorylation and blocking NFκB nuclear translocation. Eur J Pharmacol 653(1–3):8–15
doi: 10.1016/j.ejphar.2010.11.026
Kyaw MH, Kern DM, Zhou S, Tunceli O, Jafri HS, Falloon J (2015) Healthcare utilization and costs associated with S. aureus and P. aeruginosa pneumonia in the intensive care unit: a retrospective observational cohort study in a US claims database. BMC Health Serv Res 15:241. https://doi.org/10.1186/s12913-015-0917-x
doi: 10.1186/s12913-015-0917-x pubmed: 26093384 pmcid: 4475310
Labandeira-Rey M, Couzon F, Boisset S, Brown EL, Bes M, Benito Y, Barbu EM, Vazquez V, Höök M, Etienne J, Vandenesch F, Bowden MG (2007) Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science (new York, NY) 315(5815):1130–1133. https://doi.org/10.1126/science.1137165
doi: 10.1126/science.1137165
Levin-Reisman I, Ronin I, Gefen O, Braniss I, Shoresh N, Balaban NQ (2017) Antibiotic tolerance facilitates the evolution of resistance. Science (new York, NY) 355(6327):826–830. https://doi.org/10.1126/science.aaj2191
doi: 10.1126/science.aaj2191
Liu G, Liang JC, Wang XL, Li ZH, Wang W, Guo N, Wu XP, Shen FG, Xing MX, Liu LH, Li L, Liu MY, Yu L (2011) In vitro synergy of biochanin A and ciprofloxacin against clinical isolates of Staphylococcus aureus. Molecules (basel, Switzerland) 16(8):6656–6666. https://doi.org/10.3390/molecules16086656
doi: 10.3390/molecules16086656
Marathe SA, Sen M, Dasgupta I, Chakravortty D (2012) Differential modulation of intracellular survival of cytosolic and vacuolar pathogens by curcumin. Antimicrob Agents Chemother 56(11):5555–5567. https://doi.org/10.1128/aac.00496-12
doi: 10.1128/aac.00496-12 pubmed: 22890770 pmcid: 3486527
McColl K, Murray L, El-Omar E, Dickson A, El-Nujumi A, Wirz A, Kelman A, Penny C, Knill-Jones R, Hilditch T (1998) Symptomatic benefit from eradicating Helicobacter pylori infection in patients with nonulcer dyspepsia. N Engl J Med 339(26):1869–1874. https://doi.org/10.1056/nejm199812243392601
doi: 10.1056/nejm199812243392601 pubmed: 9862941
Mechler L, Herbig A, Paprotka K, Fraunholz M, Nieselt K, Bertram R (2015) A novel point mutation promotes growth phase-dependent daptomycin tolerance in Staphylococcus aureus. Antimicrob Agents Chemother 59(9):5366–5376. https://doi.org/10.1128/aac.00643-15
doi: 10.1128/aac.00643-15 pubmed: 26100694 pmcid: 4538524
Ni S, Li B, Chen F, Wei H, Mao F, Liu Y, Xu Y, Qiu X, Li X, Liu W, Hu L, Ling D, Wang M, Zheng X, Zhu J, Lan L, Li J (2018) Novel staphyloxanthin inhibitors with improved potency against multidrug resistant Staphylococcus aureus. ACS Med Chem Lett 9(3):233–237. https://doi.org/10.1021/acsmedchemlett.7b00501
doi: 10.1021/acsmedchemlett.7b00501 pubmed: 29541366 pmcid: 5846034
Pavičić M (2019) Retraction note: Can two-way direct communication protocols be considered secure? Nanosc Res Lett 14(1):242. https://doi.org/10.1186/s11671-019-3086-8
doi: 10.1186/s11671-019-3086-8
Powers ME, Kim HK, Wang Y, Bubeck Wardenburg J (2012) ADAM10 mediates vascular injury induced by Staphylococcus aureus α-hemolysin. J Infect Dis 206(3):352–356. https://doi.org/10.1093/infdis/jis192
doi: 10.1093/infdis/jis192 pubmed: 22474035 pmcid: 3392186
Qiu J, Wang D, Hua X, Feng H, Jiang Y, Xia L, Jing D, Lu J, Yu L, Deng X (2010) Subinhibitory concentrations of thymol reduce enterotoxins A and B and α-hemolysin production in Staphylococcus aureus isolates. PLoS ONE 5(3):e9736
doi: 10.1371/journal.pone.0009736
Sarkar FH, Adsule S, Padhye S, Kulkarni S, Li Y (2006) The role of genistein and synthetic derivatives of isoflavone in cancer prevention and therapy. Mini Rev Med Chem 6(4):401–407. https://doi.org/10.2174/138955706776361439
doi: 10.2174/138955706776361439 pubmed: 16613577
Shrivastava S, Shrivastava PS, Ramasamy JJJMS (2018) World health organization releases global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. J Med Soc 32(1):76
doi: 10.4103/jms.jms_25_17
Teng Z, Shi D, Liu H, Shen Z, Zha Y, Li W, Deng X, Wang J (2017) Lysionotin attenuates Staphylococcus aureus pathogenicity by inhibiting α-toxin expression. Appl Microbiol Biotechnol 101(17):6697–6703. https://doi.org/10.1007/s00253-017-8417-z
doi: 10.1007/s00253-017-8417-z pubmed: 28710557
Tran VG, Venkatasubramaniam A, Adhikari RP, Krishnan S, Wang X, Le VTM, Le HN, Vu TTT, Schneider-Smith E, Aman MJ, Diep BA (2020) Efficacy of active immunization with attenuated α-hemolysin and panton-valentine leukocidin in a rabbit model of Staphylococcus aureus necrotizing pneumonia. J Infect Dis 221(2):267–275. https://doi.org/10.1093/infdis/jiz437
doi: 10.1093/infdis/jiz437 pubmed: 31504652
Valeva A, Walev I, Pinkernell M, Walker B, Bayley H, Palmer M, Bhakdi S (1997) Transmembrane beta-barrel of staphylococcal alpha-toxin forms in sensitive but not in resistant cells. Proc Natl Acad Sci USA 94(21):11607–11611. https://doi.org/10.1073/pnas.94.21.11607
doi: 10.1073/pnas.94.21.11607 pubmed: 9326657 pmcid: 23553
Wilke GA, Bubeck Wardenburg J (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc Natl Acad Sci USA 107(30):13473–13478. https://doi.org/10.1073/pnas.1001815107
doi: 10.1073/pnas.1001815107 pubmed: 20624979 pmcid: 2922128
Wu SC, Liu F, Zhu K, Shen JJJA, Chemistry F (2019a) Natural products that target virulence factors in antibiotic-resistant Staphylococcus aureus. J Agric Food Chem 67:13195
doi: 10.1021/acs.jafc.9b05595
Wu SC, Liu F, Zhu K, Shen JZ (2019b) Natural products that target virulence factors in antibiotic-resistant Staphylococcus aureus. J Agric Food Chem 67(48):13195–13211. https://doi.org/10.1021/acs.jafc.9b05595
doi: 10.1021/acs.jafc.9b05595 pubmed: 31702908
Xia F, Li X, Wang B, Gong P, Xiao F, Yang M, Zhang L, Song J, Hu L, Cheng M, Sun C, Feng X, Lei L, Ouyang S, Liu ZJ, Li X, Gu J, Han W (2016) Combination therapy of LysGH15 and apigenin as a new strategy for treating pneumonia caused by Staphylococcus aureus. Appl Environ Microbiol 82(1):87–94. https://doi.org/10.1128/aem.02581-15
doi: 10.1128/aem.02581-15 pubmed: 26475103

Auteurs

Jiaxuan Feng (J)

Changchun University of Chinese Medicine, Changchun, 130117, China.

Dazhong Sun (D)

First School of Clinical Medicine, Guangzhou University of Chinese Medicine, Guangzhou, 510006, China.

Li Wang (L)

Changchun University of Chinese Medicine, Changchun, 130117, China.

Xueting Li (X)

Changchun University of Chinese Medicine, Changchun, 130117, China.

Jiyu Guan (J)

Key Laboratory of Zoonosis, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, 130062, China.

Lin Wei (L)

Changchun University of Chinese Medicine, Changchun, 130117, China.

Donghui Yue (D)

Changchun University of Chinese Medicine, Changchun, 130117, China.

Xingye Wang (X)

Changchun University of Chinese Medicine, Changchun, 130117, China.

Yicheng Zhao (Y)

Changchun University of Chinese Medicine, Changchun, 130117, China.

Haimiao Yang (H)

Affiliated Hospital to Changchun University of Chinese Medicine, Changchun, 130021, China.

Wu Song (W)

Changchun University of Chinese Medicine, Changchun, 130117, China. five841110@126.com.

Bingmei Wang (B)

Changchun University of Chinese Medicine, Changchun, 130117, China. bingmeiwang1970@163.com.

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