Biofilm Inhibitors That Target Amyloid Proteins

Overview

Journal Chem Biol

Publisher Elsevier

Specialties Biochemistry
Biology
Chemistry

Date 2013 Jan 29

PMID 23352144

Citations 32

Authors

Diego Romero

Edgardo Sanabria-Valentin

Hera Vlamakis

Roberto Kolter

Affiliations

Soon will be listed here.

Abstract

Bacteria establish stable communities, known as biofilms, that are resistant to antimicrobials. Biofilm robustness is due to the presence of an extracellular matrix, which for several species-among them Bacillus subtilis-includes amyloid-like protein fibers. In this work, we show that B. subtilis biofilms can be a simple and reliable tool for screening of molecules with antiamyloid activity. We identified two molecules, AA-861 and parthenolide, which efficiently inhibited biofilms by preventing the formation of amyloid-like fibers. Parthenolide also disrupted pre-established biofilms. These molecules also impeded the formation of biofilms of other bacterial species that secrete amyloid proteins, such as Bacillus cereus and Escherichia coli. Furthermore, the identified molecules decreased the conversion of the yeast protein New1 to the prion state in a heterologous host, indicating the broad range of activity of the molecules.

Citing Articles

Mechanism of antibacterial resistance, strategies and next-generation antimicrobials to contain antimicrobial resistance: a review.

Belay W, Getachew M, Tegegne B, Teffera Z, Dagne A, Zeleke T Front Pharmacol. 2024; 15:1444781.

PMID: 39221153 PMC: 11362070. DOI: 10.3389/fphar.2024.1444781.

Targeting bacterial growth in biofilm conditions: rational design of novel inhibitors to mitigate clinical and food contamination using QSAR.

Galvez-Llompart M, Hierrezuelo J, Blasco M, Zanni R, Galvez J, de Vicente A J Enzyme Inhib Med Chem. 2024; 39(1):2330907.

PMID: 38651823 PMC: 11041518. DOI: 10.1080/14756366.2024.2330907.

Contemporary strategies and approaches for characterizing composition and enhancing biofilm penetration targeting bacterial extracellular polymeric substances.

Lu L, Zhao Y, Li M, Wang X, Zhu J, Liao L J Pharm Anal. 2024; 14(4):100906.

PMID: 38634060 PMC: 11022105. DOI: 10.1016/j.jpha.2023.11.013.

Nanomaterials Regulate Bacterial Quorum Sensing: Applications, Mechanisms, and Optimization Strategies.

Hu C, He G, Yang Y, Wang N, Zhang Y, Su Y Adv Sci (Weinh). 2024; 11(15):e2306070.

PMID: 38350718 PMC: 11022734. DOI: 10.1002/advs.202306070.

Titanium complexes affect biofilm formation.

Hayet S, Ghrayeb M, Azulay D, Shpilt Z, Tshuva E, Chai L RSC Med Chem. 2023; 14(5):983-991.

PMID: 37252093 PMC: 10211322. DOI: 10.1039/d3md00075c.

References

Garrity S, Sivanathan V, Dong J, Lindquist S, Hochschild A . Conversion of a yeast prion protein to an infectious form in bacteria. Proc Natl Acad Sci U S A. 2010; 107(23):10596-601. PMC: 2890818. DOI: 10.1073/pnas.0913280107. View

OToole G, Kolter R . Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol. 1998; 28(3):449-61. DOI: 10.1046/j.1365-2958.1998.00797.x. View

Romero D, Kolter R . Will biofilm disassembly agents make it to market?. Trends Microbiol. 2011; 19(7):304-6. PMC: 3750235. DOI: 10.1016/j.tim.2011.03.003. View

Romero D, Vlamakis H, Losick R, Kolter R . An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol Microbiol. 2011; 80(5):1155-68. PMC: 3103627. DOI: 10.1111/j.1365-2958.2011.07653.x. View

Yoshimoto T, Yokoyama C, Ochi K, Yamamoto S, Maki Y, Ashida Y . 2,3,5-Trimethyl-6-(12-hydroxy-5,10-dodecadiynyl)-1,4-benzoquinone (AA861), a selective inhibitor of the 5-lipoxygenase reaction and the biosynthesis of slow-reacting substance of anaphylaxis. Biochim Biophys Acta. 1982; 713(2):470-3. View

Cegelski L, Pinkner J, Hammer N, Cusumano C, Hung C, Chorell E . Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol. 2009; 5(12):913-9. PMC: 2838449. DOI: 10.1038/nchembio.242. View

Fowler D, Koulov A, Balch W, Kelly J . Functional amyloid--from bacteria to humans. Trends Biochem Sci. 2007; 32(5):217-24. DOI: 10.1016/j.tibs.2007.03.003. View

Yasbin R, Young F . Transduction in Bacillus subtilis by bacteriophage SPP1. J Virol. 1974; 14(6):1343-8. PMC: 355660. DOI: 10.1128/JVI.14.6.1343-1348.1974. View

Dobson C . Principles of protein folding, misfolding and aggregation. Semin Cell Dev Biol. 2004; 15(1):3-16. DOI: 10.1016/j.semcdb.2003.12.008. View

10.

Romero D, Aguilar C, Losick R, Kolter R . Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci U S A. 2010; 107(5):2230-4. PMC: 2836674. DOI: 10.1073/pnas.0910560107. View

11.

Wosten H, de Vocht M . Hydrophobins, the fungal coat unravelled. Biochim Biophys Acta. 2000; 1469(2):79-86. DOI: 10.1016/s0304-4157(00)00002-2. View

12.

Tomiyama T, Kaneko H, Kataoka K, Asano S, Endo N . Rifampicin inhibits the toxicity of pre-aggregated amyloid peptides by binding to peptide fibrils and preventing amyloid-cell interaction. Biochem J. 1997; 322 ( Pt 3):859-65. PMC: 1218267. DOI: 10.1042/bj3220859. View

13.

Branda S, Chu F, Kearns D, Losick R, Kolter R . A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol. 2006; 59(4):1229-38. DOI: 10.1111/j.1365-2958.2005.05020.x. View

14.

Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R . D-amino acids trigger biofilm disassembly. Science. 2010; 328(5978):627-9. PMC: 2921573. DOI: 10.1126/science.1188628. View

15.

Claessen D, Wosten H, van Keulen G, Faber O, Alves A, Meijer W . Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic surface. Mol Microbiol. 2002; 44(6):1483-92. DOI: 10.1046/j.1365-2958.2002.02980.x. View

16.

Lopez D, Vlamakis H, Losick R, Kolter R . Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol. 2009; 74(3):609-18. PMC: 2983100. DOI: 10.1111/j.1365-2958.2009.06882.x. View

17.

Vlamakis H, Aguilar C, Losick R, Kolter R . Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev. 2008; 22(7):945-53. PMC: 2279205. DOI: 10.1101/gad.1645008. View

18.

Weggen S, ERIKSEN J, Das P, Sagi S, Wang R, Pietrzik C . A subset of NSAIDs lower amyloidogenic Abeta42 independently of cyclooxygenase activity. Nature. 2001; 414(6860):212-6. DOI: 10.1038/35102591. View

19.

Gasparini L, Rusconi L, Xu H, Del Soldato P, Ongini E . Modulation of beta-amyloid metabolism by non-steroidal anti-inflammatory drugs in neuronal cell cultures. J Neurochem. 2003; 88(2):337-48. DOI: 10.1111/j.1471-4159.2004.02154.x. View

20.

Gebbink M, Claessen D, Bouma B, Dijkhuizen L, Wosten H . Amyloids--a functional coat for microorganisms. Nat Rev Microbiol. 2005; 3(4):333-41. DOI: 10.1038/nrmicro1127. View