The physicochemical fingerprint of Necator americanus

Necator americanus, a haematophagous hookworm parasite, infects ~10% of the world’s population and is considered to be a significant public health risk. Its lifecycle has distinct stages, permitting its successful transit from the skin via the lungs (L3) to the intestinal tract (L4 maturing to adult...

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Main Authors: Chauhan, Veeren M., Scurr, David J., Christie, Thomas, Telford, Gary, Aylott, Jonathan W., Pritchard, D.I.
Format: Article
Published: Public Library of Science 2017
Subjects:
Online Access:https://eprints.nottingham.ac.uk/47366/
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author Chauhan, Veeren M.
Scurr, David J.
Christie, Thomas
Telford, Gary
Aylott, Jonathan W.
Pritchard, D.I.
author_facet Chauhan, Veeren M.
Scurr, David J.
Christie, Thomas
Telford, Gary
Aylott, Jonathan W.
Pritchard, D.I.
author_sort Chauhan, Veeren M.
building Nottingham Research Data Repository
collection Online Access
description Necator americanus, a haematophagous hookworm parasite, infects ~10% of the world’s population and is considered to be a significant public health risk. Its lifecycle has distinct stages, permitting its successful transit from the skin via the lungs (L3) to the intestinal tract (L4 maturing to adult). It has been hypothesised that the L3 larval sheath, which is shed during percutaneous infection (exsheathment), diverts the immune system to allow successful infection and reinfection in endemic areas. However, the physicochemical properties of the L3 larval cuticle and sheath, which are in direct contact with the skin and its immune defences, are unknown. In the present study, we controlled exsheathment, to characterise the sheath and underlying cuticle surfaces in situ, using atomic force microscopy (AFM) and time-of-flight secondary ion mass spectrometry (ToF-SIMS). AFM revealed previously unseen surface area enhancing nano-annuli exclusive to the sheath surface and confirmed greater adhesion forces exist between cationic surfaces and the sheath, when compared to the emergent L3 cuticle. Furthermore, ToF-SIMS elucidated different chemistries between the surfaces of the cuticle and sheath which could be of biological significance. For example, the phosphatidylglycerol rich cuticle surface may support the onward migration of a lubricated infective stage, while the anionic and potentially immunologically active heparan sulphate rich deposited sheath could result in the diversion of immune defences to an inanimate antigenic nidus. We propose that our initial studies into the surface analysis of this hookworm provides a timely insight into the physicochemical properties of a globally important human pathogen at its infective stage and anticipate that the development and application of this analytical methodology will support translation of these findings into a biological context.
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spelling nottingham-473662020-05-04T19:21:16Z https://eprints.nottingham.ac.uk/47366/ The physicochemical fingerprint of Necator americanus Chauhan, Veeren M. Scurr, David J. Christie, Thomas Telford, Gary Aylott, Jonathan W. Pritchard, D.I. Necator americanus, a haematophagous hookworm parasite, infects ~10% of the world’s population and is considered to be a significant public health risk. Its lifecycle has distinct stages, permitting its successful transit from the skin via the lungs (L3) to the intestinal tract (L4 maturing to adult). It has been hypothesised that the L3 larval sheath, which is shed during percutaneous infection (exsheathment), diverts the immune system to allow successful infection and reinfection in endemic areas. However, the physicochemical properties of the L3 larval cuticle and sheath, which are in direct contact with the skin and its immune defences, are unknown. In the present study, we controlled exsheathment, to characterise the sheath and underlying cuticle surfaces in situ, using atomic force microscopy (AFM) and time-of-flight secondary ion mass spectrometry (ToF-SIMS). AFM revealed previously unseen surface area enhancing nano-annuli exclusive to the sheath surface and confirmed greater adhesion forces exist between cationic surfaces and the sheath, when compared to the emergent L3 cuticle. Furthermore, ToF-SIMS elucidated different chemistries between the surfaces of the cuticle and sheath which could be of biological significance. For example, the phosphatidylglycerol rich cuticle surface may support the onward migration of a lubricated infective stage, while the anionic and potentially immunologically active heparan sulphate rich deposited sheath could result in the diversion of immune defences to an inanimate antigenic nidus. We propose that our initial studies into the surface analysis of this hookworm provides a timely insight into the physicochemical properties of a globally important human pathogen at its infective stage and anticipate that the development and application of this analytical methodology will support translation of these findings into a biological context. Public Library of Science 2017-12-06 Article PeerReviewed Chauhan, Veeren M., Scurr, David J., Christie, Thomas, Telford, Gary, Aylott, Jonathan W. and Pritchard, D.I. (2017) The physicochemical fingerprint of Necator americanus. PLOS Neglected Tropical Diseases, 11 (12). e0005971/1-e0005971/19. ISSN 1935-2735 Necator americanus cuticle sheath exsheathment physicochemical properties heparan sulphate http://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0005971 doi:10.1371/journal.pntd.0005971 doi:10.1371/journal.pntd.0005971
spellingShingle Necator americanus
cuticle
sheath
exsheathment
physicochemical properties
heparan sulphate
Chauhan, Veeren M.
Scurr, David J.
Christie, Thomas
Telford, Gary
Aylott, Jonathan W.
Pritchard, D.I.
The physicochemical fingerprint of Necator americanus
title The physicochemical fingerprint of Necator americanus
title_full The physicochemical fingerprint of Necator americanus
title_fullStr The physicochemical fingerprint of Necator americanus
title_full_unstemmed The physicochemical fingerprint of Necator americanus
title_short The physicochemical fingerprint of Necator americanus
title_sort physicochemical fingerprint of necator americanus
topic Necator americanus
cuticle
sheath
exsheathment
physicochemical properties
heparan sulphate
url https://eprints.nottingham.ac.uk/47366/
https://eprints.nottingham.ac.uk/47366/
https://eprints.nottingham.ac.uk/47366/