Starvation at the larval stage increases the vector competence of Aedes aegypti females for Zika virus
Aedes aegypti is the primary vector of Zika virus (ZIKV), a flavivirus which typically presents itself as febrile-like symptoms in humans but can also cause neurological and pregnancy complications. The transmission cycle of mosquito-borne arboviruses such as ZIKV requires that various key tissues i...
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description | Aedes aegypti is the primary vector of Zika virus (ZIKV), a flavivirus which typically presents itself as febrile-like symptoms in humans but can also cause neurological and pregnancy complications. The transmission cycle of mosquito-borne arboviruses such as ZIKV requires that various key tissues in the female mosquito get productively infected with the virus before the mosquito can transmit the virus to another vertebrate host. Following ingestion of a viremic blood-meal from a vertebrate, ZIKV initially infects the midgut epithelium before exiting the midgut after blood-meal digestion to disseminate to secondary tissues including the salivary glands. Here we investigated whether smaller Ae. aegypti females resulting from food deprivation as larvae exhibited an altered vector competence for blood-meal acquired ZIKV relative to larger mosquitoes. Midguts from small 'Starve' and large 'Control' Ae. aegypti were dissected to visualize by transmission electron microscopy (TEM) the midgut basal lamina (BL) as physical evidence for the midgut escape barrier showing Starve mosquitoes with a significantly thinner midgut BL than Control mosquitoes at two timepoints. ZIKV replication was inhibited in Starve mosquitoes following intrathoracic injection of virus, however, Starve mosquitoes exhibited a significantly higher midgut escape and population dissemination rate at 9 days post-infection (dpi) via blood-meal, with more virus present in saliva and head tissue than Control by 10 dpi and 14 dpi, respectively. These results indicate that Ae. aegypti developing under stressful conditions potentially exhibit higher midgut infection and dissemination rates for ZIKV as adults, Thus, variation in food intake as larvae is potentially a source for variable vector competence levels of the emerged adults for the virus. |
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The transmission cycle of mosquito-borne arboviruses such as ZIKV requires that various key tissues in the female mosquito get productively infected with the virus before the mosquito can transmit the virus to another vertebrate host. Following ingestion of a viremic blood-meal from a vertebrate, ZIKV initially infects the midgut epithelium before exiting the midgut after blood-meal digestion to disseminate to secondary tissues including the salivary glands. Here we investigated whether smaller Ae. aegypti females resulting from food deprivation as larvae exhibited an altered vector competence for blood-meal acquired ZIKV relative to larger mosquitoes. Midguts from small 'Starve' and large 'Control' Ae. aegypti were dissected to visualize by transmission electron microscopy (TEM) the midgut basal lamina (BL) as physical evidence for the midgut escape barrier showing Starve mosquitoes with a significantly thinner midgut BL than Control mosquitoes at two timepoints. ZIKV replication was inhibited in Starve mosquitoes following intrathoracic injection of virus, however, Starve mosquitoes exhibited a significantly higher midgut escape and population dissemination rate at 9 days post-infection (dpi) via blood-meal, with more virus present in saliva and head tissue than Control by 10 dpi and 14 dpi, respectively. These results indicate that Ae. aegypti developing under stressful conditions potentially exhibit higher midgut infection and dissemination rates for ZIKV as adults, Thus, variation in food intake as larvae is potentially a source for variable vector competence levels of the emerged adults for the virus.</description><identifier>ISSN: 1935-2735</identifier><identifier>ISSN: 1935-2727</identifier><identifier>EISSN: 1935-2735</identifier><identifier>DOI: 10.1371/journal.pntd.0010003</identifier><identifier>PMID: 34843483</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adults ; Aedes - growth & development ; Aedes - physiology ; Aedes - virology ; Aedes aegypti ; Animals ; Aquatic insects ; Basal lamina ; Basement Membrane - virology ; Biology and Life Sciences ; Blood ; Complications ; Control ; Culicidae ; Deprivation ; Dietary restrictions ; Electron microscopy ; Epithelium ; Experiments ; Female ; Females ; Food ; Food availability ; Food consumption ; Food intake ; Food supply ; Foods ; Gene expression ; Glands ; Humidity ; Infections ; Ingestion ; Insects ; Larva - growth & development ; Larva - physiology ; Larva - virology ; Larvae ; Medicine and Health Sciences ; Midgut ; Mosquito Vectors - growth & development ; Mosquito Vectors - physiology ; Mosquito Vectors - virology ; Mosquitoes ; Neurological complications ; Pregnancy ; Pregnancy complications ; Saliva ; Salivary gland ; Salivary glands ; Salivary Glands - virology ; Starvation ; Symptoms ; Tissue ; Tissues ; Transmission ; Transmission electron microscopy ; Tropical diseases ; Vector-borne diseases ; Vertebrates ; Viruses ; Zika virus ; Zika Virus - physiology</subject><ispartof>PLoS neglected tropical diseases, 2021-11, Vol.15 (11), p.e0010003</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Herd et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Herd et al 2021 Herd et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c624t-d424d89ec58914fa9c2e76ed08e5c9b427f3a977cda45636a5459ec0ac0ec84f3</citedby><cites>FETCH-LOGICAL-c624t-d424d89ec58914fa9c2e76ed08e5c9b427f3a977cda45636a5459ec0ac0ec84f3</cites><orcidid>0000-0002-3243-8408 ; 0000-0002-3539-1908</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8659361/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8659361/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34843483$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Bartholomay, Lyric C.</contributor><creatorcontrib>Herd, Christie S</creatorcontrib><creatorcontrib>Grant, DeAna G</creatorcontrib><creatorcontrib>Lin, Jingyi</creatorcontrib><creatorcontrib>Franz, Alexander W E</creatorcontrib><title>Starvation at the larval stage increases the vector competence of Aedes aegypti females for Zika virus</title><title>PLoS neglected tropical diseases</title><addtitle>PLoS Negl Trop Dis</addtitle><description>Aedes aegypti is the primary vector of Zika virus (ZIKV), a flavivirus which typically presents itself as febrile-like symptoms in humans but can also cause neurological and pregnancy complications. The transmission cycle of mosquito-borne arboviruses such as ZIKV requires that various key tissues in the female mosquito get productively infected with the virus before the mosquito can transmit the virus to another vertebrate host. Following ingestion of a viremic blood-meal from a vertebrate, ZIKV initially infects the midgut epithelium before exiting the midgut after blood-meal digestion to disseminate to secondary tissues including the salivary glands. Here we investigated whether smaller Ae. aegypti females resulting from food deprivation as larvae exhibited an altered vector competence for blood-meal acquired ZIKV relative to larger mosquitoes. Midguts from small 'Starve' and large 'Control' Ae. aegypti were dissected to visualize by transmission electron microscopy (TEM) the midgut basal lamina (BL) as physical evidence for the midgut escape barrier showing Starve mosquitoes with a significantly thinner midgut BL than Control mosquitoes at two timepoints. ZIKV replication was inhibited in Starve mosquitoes following intrathoracic injection of virus, however, Starve mosquitoes exhibited a significantly higher midgut escape and population dissemination rate at 9 days post-infection (dpi) via blood-meal, with more virus present in saliva and head tissue than Control by 10 dpi and 14 dpi, respectively. These results indicate that Ae. aegypti developing under stressful conditions potentially exhibit higher midgut infection and dissemination rates for ZIKV as adults, Thus, variation in food intake as larvae is potentially a source for variable vector competence levels of the emerged adults for the virus.</description><subject>Adults</subject><subject>Aedes - growth & development</subject><subject>Aedes - physiology</subject><subject>Aedes - virology</subject><subject>Aedes aegypti</subject><subject>Animals</subject><subject>Aquatic insects</subject><subject>Basal lamina</subject><subject>Basement Membrane - virology</subject><subject>Biology and Life Sciences</subject><subject>Blood</subject><subject>Complications</subject><subject>Control</subject><subject>Culicidae</subject><subject>Deprivation</subject><subject>Dietary restrictions</subject><subject>Electron microscopy</subject><subject>Epithelium</subject><subject>Experiments</subject><subject>Female</subject><subject>Females</subject><subject>Food</subject><subject>Food availability</subject><subject>Food consumption</subject><subject>Food intake</subject><subject>Food supply</subject><subject>Foods</subject><subject>Gene expression</subject><subject>Glands</subject><subject>Humidity</subject><subject>Infections</subject><subject>Ingestion</subject><subject>Insects</subject><subject>Larva - growth & development</subject><subject>Larva - physiology</subject><subject>Larva - virology</subject><subject>Larvae</subject><subject>Medicine and Health Sciences</subject><subject>Midgut</subject><subject>Mosquito Vectors - growth & development</subject><subject>Mosquito Vectors - physiology</subject><subject>Mosquito Vectors - virology</subject><subject>Mosquitoes</subject><subject>Neurological complications</subject><subject>Pregnancy</subject><subject>Pregnancy complications</subject><subject>Saliva</subject><subject>Salivary gland</subject><subject>Salivary glands</subject><subject>Salivary Glands - virology</subject><subject>Starvation</subject><subject>Symptoms</subject><subject>Tissue</subject><subject>Tissues</subject><subject>Transmission</subject><subject>Transmission electron microscopy</subject><subject>Tropical diseases</subject><subject>Vector-borne diseases</subject><subject>Vertebrates</subject><subject>Viruses</subject><subject>Zika virus</subject><subject>Zika Virus - 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growth & development</topic><topic>Aedes - physiology</topic><topic>Aedes - virology</topic><topic>Aedes aegypti</topic><topic>Animals</topic><topic>Aquatic insects</topic><topic>Basal lamina</topic><topic>Basement Membrane - virology</topic><topic>Biology and Life Sciences</topic><topic>Blood</topic><topic>Complications</topic><topic>Control</topic><topic>Culicidae</topic><topic>Deprivation</topic><topic>Dietary restrictions</topic><topic>Electron microscopy</topic><topic>Epithelium</topic><topic>Experiments</topic><topic>Female</topic><topic>Females</topic><topic>Food</topic><topic>Food availability</topic><topic>Food consumption</topic><topic>Food intake</topic><topic>Food supply</topic><topic>Foods</topic><topic>Gene expression</topic><topic>Glands</topic><topic>Humidity</topic><topic>Infections</topic><topic>Ingestion</topic><topic>Insects</topic><topic>Larva - growth & development</topic><topic>Larva - physiology</topic><topic>Larva - virology</topic><topic>Larvae</topic><topic>Medicine and Health Sciences</topic><topic>Midgut</topic><topic>Mosquito Vectors - growth & development</topic><topic>Mosquito Vectors - physiology</topic><topic>Mosquito Vectors - virology</topic><topic>Mosquitoes</topic><topic>Neurological complications</topic><topic>Pregnancy</topic><topic>Pregnancy complications</topic><topic>Saliva</topic><topic>Salivary gland</topic><topic>Salivary glands</topic><topic>Salivary Glands - virology</topic><topic>Starvation</topic><topic>Symptoms</topic><topic>Tissue</topic><topic>Tissues</topic><topic>Transmission</topic><topic>Transmission electron microscopy</topic><topic>Tropical diseases</topic><topic>Vector-borne diseases</topic><topic>Vertebrates</topic><topic>Viruses</topic><topic>Zika virus</topic><topic>Zika Virus - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Herd, Christie S</creatorcontrib><creatorcontrib>Grant, DeAna G</creatorcontrib><creatorcontrib>Lin, Jingyi</creatorcontrib><creatorcontrib>Franz, Alexander W E</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Health and Safety Science Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS neglected tropical diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Herd, Christie S</au><au>Grant, DeAna G</au><au>Lin, Jingyi</au><au>Franz, Alexander W E</au><au>Bartholomay, Lyric C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Starvation at the larval stage increases the vector competence of Aedes aegypti females for Zika virus</atitle><jtitle>PLoS neglected tropical diseases</jtitle><addtitle>PLoS Negl Trop Dis</addtitle><date>2021-11-01</date><risdate>2021</risdate><volume>15</volume><issue>11</issue><spage>e0010003</spage><pages>e0010003-</pages><issn>1935-2735</issn><issn>1935-2727</issn><eissn>1935-2735</eissn><abstract>Aedes aegypti is the primary vector of Zika virus (ZIKV), a flavivirus which typically presents itself as febrile-like symptoms in humans but can also cause neurological and pregnancy complications. The transmission cycle of mosquito-borne arboviruses such as ZIKV requires that various key tissues in the female mosquito get productively infected with the virus before the mosquito can transmit the virus to another vertebrate host. Following ingestion of a viremic blood-meal from a vertebrate, ZIKV initially infects the midgut epithelium before exiting the midgut after blood-meal digestion to disseminate to secondary tissues including the salivary glands. Here we investigated whether smaller Ae. aegypti females resulting from food deprivation as larvae exhibited an altered vector competence for blood-meal acquired ZIKV relative to larger mosquitoes. Midguts from small 'Starve' and large 'Control' Ae. aegypti were dissected to visualize by transmission electron microscopy (TEM) the midgut basal lamina (BL) as physical evidence for the midgut escape barrier showing Starve mosquitoes with a significantly thinner midgut BL than Control mosquitoes at two timepoints. ZIKV replication was inhibited in Starve mosquitoes following intrathoracic injection of virus, however, Starve mosquitoes exhibited a significantly higher midgut escape and population dissemination rate at 9 days post-infection (dpi) via blood-meal, with more virus present in saliva and head tissue than Control by 10 dpi and 14 dpi, respectively. These results indicate that Ae. aegypti developing under stressful conditions potentially exhibit higher midgut infection and dissemination rates for ZIKV as adults, Thus, variation in food intake as larvae is potentially a source for variable vector competence levels of the emerged adults for the virus.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34843483</pmid><doi>10.1371/journal.pntd.0010003</doi><orcidid>https://orcid.org/0000-0002-3243-8408</orcidid><orcidid>https://orcid.org/0000-0002-3539-1908</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adults Aedes - growth & development Aedes - physiology Aedes - virology Aedes aegypti Animals Aquatic insects Basal lamina Basement Membrane - virology Biology and Life Sciences Blood Complications Control Culicidae Deprivation Dietary restrictions Electron microscopy Epithelium Experiments Female Females Food Food availability Food consumption Food intake Food supply Foods Gene expression Glands Humidity Infections Ingestion Insects Larva - growth & development Larva - physiology Larva - virology Larvae Medicine and Health Sciences Midgut Mosquito Vectors - growth & development Mosquito Vectors - physiology Mosquito Vectors - virology Mosquitoes Neurological complications Pregnancy Pregnancy complications Saliva Salivary gland Salivary glands Salivary Glands - virology Starvation Symptoms Tissue Tissues Transmission Transmission electron microscopy Tropical diseases Vector-borne diseases Vertebrates Viruses Zika virus Zika Virus - physiology |
title | Starvation at the larval stage increases the vector competence of Aedes aegypti females for Zika virus |
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