Aedes aegypti SGS1 is critical for Plasmodium gallinaceum infection of both the mosquito midgut and salivary glands

Abstract Background The invasion of the mosquito salivary glands by Plasmodium sporozoites is a critical step that defines the success of malaria transmission and a detailed understanding of the molecules responsible for salivary gland invasion could be leveraged towards control of vector-borne path...

Full description

Bibliographic Details
Main Authors: Bianca B. Kojin, Ines Martin-Martin, Helena R. C. Araújo, Brian Bonilla, Alvaro Molina-Cruz, Eric Calvo, Margareth L. Capurro, Zach N. Adelman
Format: Article
Language:English
Published: BMC 2021-01-01
Series:Malaria Journal
Subjects:
Online Access:https://doi.org/10.1186/s12936-020-03537-6
id doaj-86f778f4fc9c4099a700856a80cd99ff
record_format Article
spelling doaj-86f778f4fc9c4099a700856a80cd99ff2021-01-10T12:58:00ZengBMCMalaria Journal1475-28752021-01-0120111510.1186/s12936-020-03537-6Aedes aegypti SGS1 is critical for Plasmodium gallinaceum infection of both the mosquito midgut and salivary glandsBianca B. Kojin0Ines Martin-Martin1Helena R. C. Araújo2Brian Bonilla3Alvaro Molina-Cruz4Eric Calvo5Margareth L. Capurro6Zach N. Adelman7Department of Entomology and Agrilife Research, Texas A&M UniversityLaboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of HealthDepartamento de Parasitologia, Laboratório de Mosquitos Geneticamente Modificados, Instituto de Ciências Biomédicas, Universidade de São PauloLaboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of HealthLaboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of HealthLaboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of HealthDepartamento de Parasitologia, Laboratório de Mosquitos Geneticamente Modificados, Instituto de Ciências Biomédicas, Universidade de São PauloDepartment of Entomology and Agrilife Research, Texas A&M UniversityAbstract Background The invasion of the mosquito salivary glands by Plasmodium sporozoites is a critical step that defines the success of malaria transmission and a detailed understanding of the molecules responsible for salivary gland invasion could be leveraged towards control of vector-borne pathogens. Antibodies directed against the mosquito salivary gland protein SGS1 have been shown to reduce Plasmodium gallinaceum sporozoite invasion of Aedes aegypti salivary glands, but the specific role of this protein in sporozoite invasion and in other stages of the Plasmodium life cycle remains unknown. Methods RNA interference and CRISPR/Cas9 were used to evaluate the role of A. aegypti SGS1 in the P. gallinaceum life cycle. Results Knockdown and knockout of SGS1 disrupted sporozoite invasion of the salivary gland. Interestingly, mosquitoes lacking SGS1 also displayed fewer oocysts. Proteomic analyses confirmed the abolishment of SGS1 in the salivary gland of SGS1 knockout mosquitoes and revealed that the C-terminus of the protein is absent in the salivary gland of control mosquitoes. In silico analyses indicated that SGS1 contains two potential internal cleavage sites and thus might generate three proteins. Conclusion SGS1 facilitates, but is not essential for, invasion of A. aegypti salivary glands by P. gallinaceum and has a dual role as a facilitator of parasite development in the mosquito midgut. SGS1 could, therefore, be part of a strategy to decrease malaria transmission by the mosquito vector, for example in a transgenic mosquito that blocks its interaction with the parasite.https://doi.org/10.1186/s12936-020-03537-6Aedes aegyptiPlasmodium gallinaceumMalariaSalivary glandSGS1Sporozoites
collection DOAJ
language English
format Article
sources DOAJ
author Bianca B. Kojin
Ines Martin-Martin
Helena R. C. Araújo
Brian Bonilla
Alvaro Molina-Cruz
Eric Calvo
Margareth L. Capurro
Zach N. Adelman
spellingShingle Bianca B. Kojin
Ines Martin-Martin
Helena R. C. Araújo
Brian Bonilla
Alvaro Molina-Cruz
Eric Calvo
Margareth L. Capurro
Zach N. Adelman
Aedes aegypti SGS1 is critical for Plasmodium gallinaceum infection of both the mosquito midgut and salivary glands
Malaria Journal
Aedes aegypti
Plasmodium gallinaceum
Malaria
Salivary gland
SGS1
Sporozoites
author_facet Bianca B. Kojin
Ines Martin-Martin
Helena R. C. Araújo
Brian Bonilla
Alvaro Molina-Cruz
Eric Calvo
Margareth L. Capurro
Zach N. Adelman
author_sort Bianca B. Kojin
title Aedes aegypti SGS1 is critical for Plasmodium gallinaceum infection of both the mosquito midgut and salivary glands
title_short Aedes aegypti SGS1 is critical for Plasmodium gallinaceum infection of both the mosquito midgut and salivary glands
title_full Aedes aegypti SGS1 is critical for Plasmodium gallinaceum infection of both the mosquito midgut and salivary glands
title_fullStr Aedes aegypti SGS1 is critical for Plasmodium gallinaceum infection of both the mosquito midgut and salivary glands
title_full_unstemmed Aedes aegypti SGS1 is critical for Plasmodium gallinaceum infection of both the mosquito midgut and salivary glands
title_sort aedes aegypti sgs1 is critical for plasmodium gallinaceum infection of both the mosquito midgut and salivary glands
publisher BMC
series Malaria Journal
issn 1475-2875
publishDate 2021-01-01
description Abstract Background The invasion of the mosquito salivary glands by Plasmodium sporozoites is a critical step that defines the success of malaria transmission and a detailed understanding of the molecules responsible for salivary gland invasion could be leveraged towards control of vector-borne pathogens. Antibodies directed against the mosquito salivary gland protein SGS1 have been shown to reduce Plasmodium gallinaceum sporozoite invasion of Aedes aegypti salivary glands, but the specific role of this protein in sporozoite invasion and in other stages of the Plasmodium life cycle remains unknown. Methods RNA interference and CRISPR/Cas9 were used to evaluate the role of A. aegypti SGS1 in the P. gallinaceum life cycle. Results Knockdown and knockout of SGS1 disrupted sporozoite invasion of the salivary gland. Interestingly, mosquitoes lacking SGS1 also displayed fewer oocysts. Proteomic analyses confirmed the abolishment of SGS1 in the salivary gland of SGS1 knockout mosquitoes and revealed that the C-terminus of the protein is absent in the salivary gland of control mosquitoes. In silico analyses indicated that SGS1 contains two potential internal cleavage sites and thus might generate three proteins. Conclusion SGS1 facilitates, but is not essential for, invasion of A. aegypti salivary glands by P. gallinaceum and has a dual role as a facilitator of parasite development in the mosquito midgut. SGS1 could, therefore, be part of a strategy to decrease malaria transmission by the mosquito vector, for example in a transgenic mosquito that blocks its interaction with the parasite.
topic Aedes aegypti
Plasmodium gallinaceum
Malaria
Salivary gland
SGS1
Sporozoites
url https://doi.org/10.1186/s12936-020-03537-6
work_keys_str_mv AT biancabkojin aedesaegyptisgs1iscriticalforplasmodiumgallinaceuminfectionofboththemosquitomidgutandsalivaryglands
AT inesmartinmartin aedesaegyptisgs1iscriticalforplasmodiumgallinaceuminfectionofboththemosquitomidgutandsalivaryglands
AT helenarcaraujo aedesaegyptisgs1iscriticalforplasmodiumgallinaceuminfectionofboththemosquitomidgutandsalivaryglands
AT brianbonilla aedesaegyptisgs1iscriticalforplasmodiumgallinaceuminfectionofboththemosquitomidgutandsalivaryglands
AT alvaromolinacruz aedesaegyptisgs1iscriticalforplasmodiumgallinaceuminfectionofboththemosquitomidgutandsalivaryglands
AT ericcalvo aedesaegyptisgs1iscriticalforplasmodiumgallinaceuminfectionofboththemosquitomidgutandsalivaryglands
AT margarethlcapurro aedesaegyptisgs1iscriticalforplasmodiumgallinaceuminfectionofboththemosquitomidgutandsalivaryglands
AT zachnadelman aedesaegyptisgs1iscriticalforplasmodiumgallinaceuminfectionofboththemosquitomidgutandsalivaryglands
_version_ 1724341991759675392