TCF-ALP: A fluorescent probe for the selective detection of: Staphylococcus bacteria and application in "smart" wound dressings

Lauren Gwynne; George T. Williams; Kai Cheng Yan; Bethany L. Patenall; Jordan E. Gardiner; Xiao Peng He; Jean Yves Maillard; Tony D. James; Adam C. Sedgwick; A. Toby A. Jenkins

doi:10.1039/d0bm01918f

TCF-ALP: A fluorescent probe for the selective detection of: Staphylococcus bacteria and application in "smart" wound dressings

Lauren Gwynne, George T. Williams, Kai Cheng Yan, Bethany L. Patenall, Jordan E. Gardiner, Xiao Peng He, Jean Yves Maillard, Tony D. James, Adam C. Sedgwick, A. Toby A. Jenkins

Department of Chemistry

Research output: Contribution to journal › Article › peer-review

16 Citations (SciVal)

Abstract

Alkaline phosphatase (ALP) is an important enzyme-based biomarker present in several bacterial species; however, it is currently undervalued as a strategy to detect pathogenic bacteria. Here, we explore our ALP-responsive colorimetric and fluorescent probe (TCF-ALP) for such applications. TCF-ALP displayed a colorimetric and fluorescence response towards Staphylococcus aureus (S. aureus), with a limit of detection of 3.7 × 106 CFU mL-1 after 24 h incubation. To our surprise, TCF-ALP proved selective towards Staphylococcus bacteria when compared with Enterococcus faecalis (E. faecalis), and Gram-negative P. aeruginosa and E. coli. Selectivity was also seen in clinically relevant S. aureus biofilms. Owing to the high prevalence and surface location of S. aureus in chronic wounds, TCF-ALP was subsequently encapsulated in polyvinyl alcohol (PVA)-based hydrogels as a proof-of-concept "smart"wound dressing. TCF-ALP hydrogels were capable of detecting S. aureus in planktonic and biofilm assays, and displayed a clear colour change from yellow to purple after 24 h incubation using ex vivo porcine skin models. Overall, TCF-ALP is a simple tool that requires no prior knowledge, training, or specialist equipment, and has the potential to overcome issues related to invasive swabbing and tissue biopsy methods. Thus, TCF-ALP could be used as a tool to monitor the early development of infection in a wound and allow for the rapid provision of appropriate treatment for Staphylococcal bacterial infections.

Original language	English
Pages (from-to)	4433-4439
Number of pages	7
Journal	Biomaterials Science
Volume	9
Issue number	12
Early online date	11 May 2021
DOIs	https://doi.org/10.1039/d0bm01918f
Publication status	Published - 21 Jun 2021

Bibliographical note

Funding Information:
This work was supported in part by grant MR/N0137941/1 for the GW4 BIOMED DTP, awarded to the Universities of Bath, Bristol, Cardiff and Exeter from the Medical Research Council (MRC)/UKRI. The authors thank the National Natural Science Foundation of China (No. 21788102, 91853201, 21722801, 81673489 and 31871414), the Shanghai Municipal Science and Technology Major Project (No. 2018SHZDZX03), the International Cooperation Program of Shanghai Science and Technology Committee (No. 17520750100) and the Fundamental Research Funds for the Central Universities (222201717003) for financial support. LG and ATAJ would like to thank Dr Maisem Laabei for his help in acquiring S. aureus strains for testing. GW would like to thank the GCDC at the University of Kent for funding. The authors would like to thank Kaya Davies-Brenchley for her help in the preparation of this manuscript. ACS would like to extend his thanks to Sajal Sen (The University of Texas at Austin) and James T. Brewster (Harvard University) for helpful discussions. TDJ wishes to thank the Royal Society for a Wolfson Research Merit Award and the Open Research Fund of the School of Chemistry and Chemical Engineering, Henan Normal University for support (2020ZD01).

ASJC Scopus subject areas

Biomedical Engineering
General Materials Science

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Cite this

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title = "TCF-ALP: A fluorescent probe for the selective detection of: Staphylococcus bacteria and application in {"}smart{"} wound dressings",

abstract = "Alkaline phosphatase (ALP) is an important enzyme-based biomarker present in several bacterial species; however, it is currently undervalued as a strategy to detect pathogenic bacteria. Here, we explore our ALP-responsive colorimetric and fluorescent probe (TCF-ALP) for such applications. TCF-ALP displayed a colorimetric and fluorescence response towards Staphylococcus aureus (S. aureus), with a limit of detection of 3.7 × 106 CFU mL-1 after 24 h incubation. To our surprise, TCF-ALP proved selective towards Staphylococcus bacteria when compared with Enterococcus faecalis (E. faecalis), and Gram-negative P. aeruginosa and E. coli. Selectivity was also seen in clinically relevant S. aureus biofilms. Owing to the high prevalence and surface location of S. aureus in chronic wounds, TCF-ALP was subsequently encapsulated in polyvinyl alcohol (PVA)-based hydrogels as a proof-of-concept {"}smart{"}wound dressing. TCF-ALP hydrogels were capable of detecting S. aureus in planktonic and biofilm assays, and displayed a clear colour change from yellow to purple after 24 h incubation using ex vivo porcine skin models. Overall, TCF-ALP is a simple tool that requires no prior knowledge, training, or specialist equipment, and has the potential to overcome issues related to invasive swabbing and tissue biopsy methods. Thus, TCF-ALP could be used as a tool to monitor the early development of infection in a wound and allow for the rapid provision of appropriate treatment for Staphylococcal bacterial infections. ",

author = "Lauren Gwynne and Williams, {George T.} and Yan, {Kai Cheng} and Patenall, {Bethany L.} and Gardiner, {Jordan E.} and He, {Xiao Peng} and Maillard, {Jean Yves} and James, {Tony D.} and Sedgwick, {Adam C.} and Jenkins, {A. Toby A.}",

note = "Funding Information: This work was supported in part by grant MR/N0137941/1 for the GW4 BIOMED DTP, awarded to the Universities of Bath, Bristol, Cardiff and Exeter from the Medical Research Council (MRC)/UKRI. The authors thank the National Natural Science Foundation of China (No. 21788102, 91853201, 21722801, 81673489 and 31871414), the Shanghai Municipal Science and Technology Major Project (No. 2018SHZDZX03), the International Cooperation Program of Shanghai Science and Technology Committee (No. 17520750100) and the Fundamental Research Funds for the Central Universities (222201717003) for financial support. LG and ATAJ would like to thank Dr Maisem Laabei for his help in acquiring S. aureus strains for testing. GW would like to thank the GCDC at the University of Kent for funding. The authors would like to thank Kaya Davies-Brenchley for her help in the preparation of this manuscript. ACS would like to extend his thanks to Sajal Sen (The University of Texas at Austin) and James T. Brewster (Harvard University) for helpful discussions. TDJ wishes to thank the Royal Society for a Wolfson Research Merit Award and the Open Research Fund of the School of Chemistry and Chemical Engineering, Henan Normal University for support (2020ZD01). ",

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AU - Gwynne, Lauren

AU - Williams, George T.

AU - Yan, Kai Cheng

AU - Patenall, Bethany L.

AU - Gardiner, Jordan E.

AU - He, Xiao Peng

AU - Maillard, Jean Yves

AU - James, Tony D.

AU - Sedgwick, Adam C.

AU - Jenkins, A. Toby A.

N1 - Funding Information: This work was supported in part by grant MR/N0137941/1 for the GW4 BIOMED DTP, awarded to the Universities of Bath, Bristol, Cardiff and Exeter from the Medical Research Council (MRC)/UKRI. The authors thank the National Natural Science Foundation of China (No. 21788102, 91853201, 21722801, 81673489 and 31871414), the Shanghai Municipal Science and Technology Major Project (No. 2018SHZDZX03), the International Cooperation Program of Shanghai Science and Technology Committee (No. 17520750100) and the Fundamental Research Funds for the Central Universities (222201717003) for financial support. LG and ATAJ would like to thank Dr Maisem Laabei for his help in acquiring S. aureus strains for testing. GW would like to thank the GCDC at the University of Kent for funding. The authors would like to thank Kaya Davies-Brenchley for her help in the preparation of this manuscript. ACS would like to extend his thanks to Sajal Sen (The University of Texas at Austin) and James T. Brewster (Harvard University) for helpful discussions. TDJ wishes to thank the Royal Society for a Wolfson Research Merit Award and the Open Research Fund of the School of Chemistry and Chemical Engineering, Henan Normal University for support (2020ZD01).

PY - 2021/6/21

Y1 - 2021/6/21

N2 - Alkaline phosphatase (ALP) is an important enzyme-based biomarker present in several bacterial species; however, it is currently undervalued as a strategy to detect pathogenic bacteria. Here, we explore our ALP-responsive colorimetric and fluorescent probe (TCF-ALP) for such applications. TCF-ALP displayed a colorimetric and fluorescence response towards Staphylococcus aureus (S. aureus), with a limit of detection of 3.7 × 106 CFU mL-1 after 24 h incubation. To our surprise, TCF-ALP proved selective towards Staphylococcus bacteria when compared with Enterococcus faecalis (E. faecalis), and Gram-negative P. aeruginosa and E. coli. Selectivity was also seen in clinically relevant S. aureus biofilms. Owing to the high prevalence and surface location of S. aureus in chronic wounds, TCF-ALP was subsequently encapsulated in polyvinyl alcohol (PVA)-based hydrogels as a proof-of-concept "smart"wound dressing. TCF-ALP hydrogels were capable of detecting S. aureus in planktonic and biofilm assays, and displayed a clear colour change from yellow to purple after 24 h incubation using ex vivo porcine skin models. Overall, TCF-ALP is a simple tool that requires no prior knowledge, training, or specialist equipment, and has the potential to overcome issues related to invasive swabbing and tissue biopsy methods. Thus, TCF-ALP could be used as a tool to monitor the early development of infection in a wound and allow for the rapid provision of appropriate treatment for Staphylococcal bacterial infections.

AB - Alkaline phosphatase (ALP) is an important enzyme-based biomarker present in several bacterial species; however, it is currently undervalued as a strategy to detect pathogenic bacteria. Here, we explore our ALP-responsive colorimetric and fluorescent probe (TCF-ALP) for such applications. TCF-ALP displayed a colorimetric and fluorescence response towards Staphylococcus aureus (S. aureus), with a limit of detection of 3.7 × 106 CFU mL-1 after 24 h incubation. To our surprise, TCF-ALP proved selective towards Staphylococcus bacteria when compared with Enterococcus faecalis (E. faecalis), and Gram-negative P. aeruginosa and E. coli. Selectivity was also seen in clinically relevant S. aureus biofilms. Owing to the high prevalence and surface location of S. aureus in chronic wounds, TCF-ALP was subsequently encapsulated in polyvinyl alcohol (PVA)-based hydrogels as a proof-of-concept "smart"wound dressing. TCF-ALP hydrogels were capable of detecting S. aureus in planktonic and biofilm assays, and displayed a clear colour change from yellow to purple after 24 h incubation using ex vivo porcine skin models. Overall, TCF-ALP is a simple tool that requires no prior knowledge, training, or specialist equipment, and has the potential to overcome issues related to invasive swabbing and tissue biopsy methods. Thus, TCF-ALP could be used as a tool to monitor the early development of infection in a wound and allow for the rapid provision of appropriate treatment for Staphylococcal bacterial infections.

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TCF-ALP: A fluorescent probe for the selective detection of: Staphylococcus bacteria and application in "smart" wound dressings

Abstract

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