Histological confinement of transglutaminase-mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse, Pediculus humanus capitis

Abstract Background Head louse females secrete liquid gel, which is mainly composed of the louse nit sheath protein 1 (LNSP1) and LNSP2, when they lay eggs. The gel is crosslinked by transglutaminase (TG) to form the nit sheath, which covers most of the egg except the top operculum area where breath...

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Main Authors: Ju Hyeon Kim, Do Eun Lee, Sang Youn Park, John M. Clark, Si Hyeock Lee
Format: Article
Language:English
Published: BMC 2023-03-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-023-05720-5
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author Ju Hyeon Kim
Do Eun Lee
Sang Youn Park
John M. Clark
Si Hyeock Lee
author_facet Ju Hyeon Kim
Do Eun Lee
Sang Youn Park
John M. Clark
Si Hyeock Lee
author_sort Ju Hyeon Kim
collection DOAJ
description Abstract Background Head louse females secrete liquid gel, which is mainly composed of the louse nit sheath protein 1 (LNSP1) and LNSP2, when they lay eggs. The gel is crosslinked by transglutaminase (TG) to form the nit sheath, which covers most of the egg except the top operculum area where breathing holes are located. Knowledge on the selective mechanism of nit sheath solidification to avoid uncontrolled crosslinking could lead to designing a novel method of louse control, but no information is available yet. Methods To elucidate the crosslinking mechanisms of nit sheath gel inside the reproductive system of head louse females, in situ hybridization in conjunction with microscopic observation of the oviposition process was conducted. Results Histochemical analysis revealed that LNSP1 and LNSP2 are expressed over the entire area of the accessory gland and uterus, whereas TG expression site is confined to a highly localized area around the opening of posterior oviduct. Detailed microscopic observations of oviposition process uncovered that a mature egg is positioned in the uterus after ovulation. Once aligned inside the uterus, the mature egg is redirected so that its operculum side is tightly held by the ventral end of the uterus being positioned toward the head again and its pointed bottom end being positioned toward the dorsal end of the uterus, which functions as a reservoir for the nit sheath gel. Conclusions Physical separation of the TG-mediated crosslinking site from the ventral end of the uterus is necessary to avoid uncontrolled crosslinking inside the uterus and to ensure selective crosslinking over only the lower part of egg without any unwanted crosslinking over the operculum during oviposition. Graphical Abstract
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spelling doaj.art-d6f5396a5baf4c9685a5c20fa0c65f552023-03-22T10:33:55ZengBMCParasites & Vectors1756-33052023-03-011611710.1186/s13071-023-05720-5Histological confinement of transglutaminase-mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse, Pediculus humanus capitisJu Hyeon Kim0Do Eun Lee1Sang Youn Park2John M. Clark3Si Hyeock Lee4Department of Tropical Medicine and Parasitology, Seoul National University College of MedicineDepartment of Agricultural Biotechnology, Seoul National UniversitySchool of Systems Biomedical Science, Soongsil UniversityDepartment of Veterinary and Animal Sciences, University of MassachusettsDepartment of Agricultural Biotechnology, Seoul National UniversityAbstract Background Head louse females secrete liquid gel, which is mainly composed of the louse nit sheath protein 1 (LNSP1) and LNSP2, when they lay eggs. The gel is crosslinked by transglutaminase (TG) to form the nit sheath, which covers most of the egg except the top operculum area where breathing holes are located. Knowledge on the selective mechanism of nit sheath solidification to avoid uncontrolled crosslinking could lead to designing a novel method of louse control, but no information is available yet. Methods To elucidate the crosslinking mechanisms of nit sheath gel inside the reproductive system of head louse females, in situ hybridization in conjunction with microscopic observation of the oviposition process was conducted. Results Histochemical analysis revealed that LNSP1 and LNSP2 are expressed over the entire area of the accessory gland and uterus, whereas TG expression site is confined to a highly localized area around the opening of posterior oviduct. Detailed microscopic observations of oviposition process uncovered that a mature egg is positioned in the uterus after ovulation. Once aligned inside the uterus, the mature egg is redirected so that its operculum side is tightly held by the ventral end of the uterus being positioned toward the head again and its pointed bottom end being positioned toward the dorsal end of the uterus, which functions as a reservoir for the nit sheath gel. Conclusions Physical separation of the TG-mediated crosslinking site from the ventral end of the uterus is necessary to avoid uncontrolled crosslinking inside the uterus and to ensure selective crosslinking over only the lower part of egg without any unwanted crosslinking over the operculum during oviposition. Graphical Abstracthttps://doi.org/10.1186/s13071-023-05720-5Head louseNitEgg sheathLNSPTransglutaminaseOviposition
spellingShingle Ju Hyeon Kim
Do Eun Lee
Sang Youn Park
John M. Clark
Si Hyeock Lee
Histological confinement of transglutaminase-mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse, Pediculus humanus capitis
Parasites & Vectors
Head louse
Nit
Egg sheath
LNSP
Transglutaminase
Oviposition
title Histological confinement of transglutaminase-mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse, Pediculus humanus capitis
title_full Histological confinement of transglutaminase-mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse, Pediculus humanus capitis
title_fullStr Histological confinement of transglutaminase-mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse, Pediculus humanus capitis
title_full_unstemmed Histological confinement of transglutaminase-mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse, Pediculus humanus capitis
title_short Histological confinement of transglutaminase-mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse, Pediculus humanus capitis
title_sort histological confinement of transglutaminase mediated nit sheath crosslinking is essential for proper oviposition and egg coating in the human head louse pediculus humanus capitis
topic Head louse
Nit
Egg sheath
LNSP
Transglutaminase
Oviposition
url https://doi.org/10.1186/s13071-023-05720-5
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