Enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating Honokiol: a comprehensive solution for biofilm-associated lung infections
Abstract Background Biofilm-associated lung infections, particularly those caused by Staphylococcus aureus (S. aureus), pose significant clinical challenges to conventional therapies. S. aureus Biofilm infections are refractory to treatment due to the presence of persister bacterial cells and the ba...
Saved in:
Main Authors: | , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2025-02-01
|
Series: | Journal of Nanobiotechnology |
Subjects: | |
Online Access: | https://doi.org/10.1186/s12951-025-03144-0 |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1823861659109687296 |
---|---|
author | Shiyu Lin Xiaojuan Li Wei Zhang Gang Shu Tim Tolker-Nielsen Haohuan Li Funeng Xu Juchun Lin Guangneng Peng Li Zhang Hualin Fu |
author_facet | Shiyu Lin Xiaojuan Li Wei Zhang Gang Shu Tim Tolker-Nielsen Haohuan Li Funeng Xu Juchun Lin Guangneng Peng Li Zhang Hualin Fu |
author_sort | Shiyu Lin |
collection | DOAJ |
description | Abstract Background Biofilm-associated lung infections, particularly those caused by Staphylococcus aureus (S. aureus), pose significant clinical challenges to conventional therapies. S. aureus Biofilm infections are refractory to treatment due to the presence of persister bacterial cells and the barrier effect of unique extracellular polymeric substances (EPS). Results This study describes the development of multifunctional micelles, HK-SL Ms, utilizing sophorolipid (SL) to encapsulate Honokiol (HK). HK-SL Ms potently disrupted the EPS barrier, killed some internal colonizing bacteria, and inhibited further bacterial adhesion. Consequently, the dynamic cycling of biofilms was hindered, achieving a promising removal of S. aureus biofilms. In vitro studies demonstrated that HK-SL Ms exhibited significant antimicrobial reduction of a 6.42 log10CFU/mL. HK-SL Ms eradicated 71.73% of biofilms by targeting extracellular polysaccharides, extracellular proteins, and viable cells within the biofilm. Additionally, 1.66 log10CFU/mL units of S. aureus within biofilms were killed. Moreover, HK-SL Ms inhibited 91.10% of early S. aureus biofilm formation by obstructing initial bacterial adhesion and the formation of extracellular polysaccharides and polysaccharide intercellular adhesins (PIA). Thus, the reestablishment and reinfection of S. aureus biofilms could be resolved promisingly. Biofilm infections are as predominant in acute pneumonia as in chronic cases, inducing similar lung inflammation. In a murine model of pneumonia infected by S. aureus, HK-SL Ms significantly reduced the bacterial load in the lungs, decreased inflammatory factor levels, and repaired lung tissue damage. Conclusions HK-SL Ms offers a novel strategy for the clinical treatment of biofilm-associated infections by dispersing and removing S. aureus biofilms and preventing new infections. Graphical Abstract |
format | Article |
id | doaj-art-8f9ce4f0d07b4c129c2abbe2137b43da |
institution | Kabale University |
issn | 1477-3155 |
language | English |
publishDate | 2025-02-01 |
publisher | BMC |
record_format | Article |
series | Journal of Nanobiotechnology |
spelling | doaj-art-8f9ce4f0d07b4c129c2abbe2137b43da2025-02-09T12:53:02ZengBMCJournal of Nanobiotechnology1477-31552025-02-0123111610.1186/s12951-025-03144-0Enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating Honokiol: a comprehensive solution for biofilm-associated lung infectionsShiyu Lin0Xiaojuan Li1Wei Zhang2Gang Shu3Tim Tolker-Nielsen4Haohuan Li5Funeng Xu6Juchun Lin7Guangneng Peng8Li Zhang9Hualin Fu10Innovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversityInnovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversityInnovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversityInnovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversityDepartment of Immunology and Microbiology, Costerton Biofilm Center, University of CopenhagenInnovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversityInnovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversityInnovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversityInnovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversitySichuan Academy of Chinese Medicine SciencesInnovative Engineering Research Center of Veterinary Pharmaceutics,, Department of Pharmacy, College of Veterinary Medicine, Sichuan Agricultural UniversityAbstract Background Biofilm-associated lung infections, particularly those caused by Staphylococcus aureus (S. aureus), pose significant clinical challenges to conventional therapies. S. aureus Biofilm infections are refractory to treatment due to the presence of persister bacterial cells and the barrier effect of unique extracellular polymeric substances (EPS). Results This study describes the development of multifunctional micelles, HK-SL Ms, utilizing sophorolipid (SL) to encapsulate Honokiol (HK). HK-SL Ms potently disrupted the EPS barrier, killed some internal colonizing bacteria, and inhibited further bacterial adhesion. Consequently, the dynamic cycling of biofilms was hindered, achieving a promising removal of S. aureus biofilms. In vitro studies demonstrated that HK-SL Ms exhibited significant antimicrobial reduction of a 6.42 log10CFU/mL. HK-SL Ms eradicated 71.73% of biofilms by targeting extracellular polysaccharides, extracellular proteins, and viable cells within the biofilm. Additionally, 1.66 log10CFU/mL units of S. aureus within biofilms were killed. Moreover, HK-SL Ms inhibited 91.10% of early S. aureus biofilm formation by obstructing initial bacterial adhesion and the formation of extracellular polysaccharides and polysaccharide intercellular adhesins (PIA). Thus, the reestablishment and reinfection of S. aureus biofilms could be resolved promisingly. Biofilm infections are as predominant in acute pneumonia as in chronic cases, inducing similar lung inflammation. In a murine model of pneumonia infected by S. aureus, HK-SL Ms significantly reduced the bacterial load in the lungs, decreased inflammatory factor levels, and repaired lung tissue damage. Conclusions HK-SL Ms offers a novel strategy for the clinical treatment of biofilm-associated infections by dispersing and removing S. aureus biofilms and preventing new infections. Graphical Abstracthttps://doi.org/10.1186/s12951-025-03144-0Staphylococcus aureus biofilmSophorolipidHonokiolNanomicelle |
spellingShingle | Shiyu Lin Xiaojuan Li Wei Zhang Gang Shu Tim Tolker-Nielsen Haohuan Li Funeng Xu Juchun Lin Guangneng Peng Li Zhang Hualin Fu Enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating Honokiol: a comprehensive solution for biofilm-associated lung infections Journal of Nanobiotechnology Staphylococcus aureus biofilm Sophorolipid Honokiol Nanomicelle |
title | Enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating Honokiol: a comprehensive solution for biofilm-associated lung infections |
title_full | Enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating Honokiol: a comprehensive solution for biofilm-associated lung infections |
title_fullStr | Enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating Honokiol: a comprehensive solution for biofilm-associated lung infections |
title_full_unstemmed | Enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating Honokiol: a comprehensive solution for biofilm-associated lung infections |
title_short | Enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating Honokiol: a comprehensive solution for biofilm-associated lung infections |
title_sort | enhanced penetration and biofilm eradication by sophorolipid micelles encapsulating honokiol a comprehensive solution for biofilm associated lung infections |
topic | Staphylococcus aureus biofilm Sophorolipid Honokiol Nanomicelle |
url | https://doi.org/10.1186/s12951-025-03144-0 |
work_keys_str_mv | AT shiyulin enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT xiaojuanli enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT weizhang enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT gangshu enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT timtolkernielsen enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT haohuanli enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT funengxu enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT juchunlin enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT guangnengpeng enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT lizhang enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections AT hualinfu enhancedpenetrationandbiofilmeradicationbysophorolipidmicellesencapsulatinghonokiolacomprehensivesolutionforbiofilmassociatedlunginfections |