Morphological and proteomic characterization of midgut of the malaria vector Anopheles albimanus at early time after a blood feeding

The midgut of anopheline mosquito is the entry of Plasmodium, the causative agent of malaria.When the mosquito feeds on parasite infected host, Plasmodium parasites reach the midgut and must confront digestive enzymes, the innate immune response and go across the peritrophic matrix (PM), a thick ext...

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Veröffentlicht in:Journal of proteomics 2014-12, Vol.111, p.100-112
Hauptverfasser: Cázares-Raga, F.E., Chávez-Munguía, B., González-Calixto, C., Ochoa-Franco, A.P., Gawinowicz, M.A., Rodríguez, M.H., Hernández-Hernández, F.C.
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creator Cázares-Raga, F.E.
Chávez-Munguía, B.
González-Calixto, C.
Ochoa-Franco, A.P.
Gawinowicz, M.A.
Rodríguez, M.H.
Hernández-Hernández, F.C.
description The midgut of anopheline mosquito is the entry of Plasmodium, the causative agent of malaria.When the mosquito feeds on parasite infected host, Plasmodium parasites reach the midgut and must confront digestive enzymes, the innate immune response and go across the peritrophic matrix (PM), a thick extracellular sheath secreted by the mosquito midgut epithelial cells. Then, to continue its development, the parasite must reach the salivary glands to achieve transmission to a vertebrate host. We report here the morphological and biochemical descriptions of the midgut changes after a blood meal in Anopheles albimanus. Before blood feeding, midgut epithelial cells contained numerous electrondense vesicles distributed in the central to apical side. These vesicles were secreted to the luminal side of the midgut after a blood meal. At early times after blood ingest, the PM is formed near microvilli as a granulous amorphous material and after it consolidates forming a highly organized fibrillar structure, constituted by layers of electrondense and electronlucent regions. Proteomic comparative analysis of sugar and blood fed midguts showed several molecules that modify their abundance after blood intake; these include innate immunity, cytoskeletal, stress response, signaling, and digestive, detoxifying and metabolism enzymes. Biological significance In the midgut of mosquitoes during bloodfeeding, many simultaneous processes occur, including digestion, innate immune activities, cytoskeleton modifications, construction of a peritrophic matrix and hormone production, between others. Mechanical forces are very intense during bloodfeeding and epithelial and muscular cells must resist the stress, modifying the actin cytoskeleton and coordinating intracellular responses by signaling. Microorganisms present in midgut contents reproduce and interact with epithelial cells triggering innate immune response. When infectious agents are present in the blood meal they must traverse the peritrophic matrix, an envelope formed from secretion products of epithelial cells, and evade the immune system in order to reach the epithelium and continue their journey towards salivary glands, in preparation for the transmission to the new hosts. During all these processes, proteins of mosquitoes are modified in order to deal with mechanical and biological challenges, and the aim of this work is to study these changes. This article is part of a Special Issue entitled: Proteomics, mass spectrometr
doi_str_mv 10.1016/j.jprot.2014.07.037
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Then, to continue its development, the parasite must reach the salivary glands to achieve transmission to a vertebrate host. We report here the morphological and biochemical descriptions of the midgut changes after a blood meal in Anopheles albimanus. Before blood feeding, midgut epithelial cells contained numerous electrondense vesicles distributed in the central to apical side. These vesicles were secreted to the luminal side of the midgut after a blood meal. At early times after blood ingest, the PM is formed near microvilli as a granulous amorphous material and after it consolidates forming a highly organized fibrillar structure, constituted by layers of electrondense and electronlucent regions. Proteomic comparative analysis of sugar and blood fed midguts showed several molecules that modify their abundance after blood intake; these include innate immunity, cytoskeletal, stress response, signaling, and digestive, detoxifying and metabolism enzymes. Biological significance In the midgut of mosquitoes during bloodfeeding, many simultaneous processes occur, including digestion, innate immune activities, cytoskeleton modifications, construction of a peritrophic matrix and hormone production, between others. Mechanical forces are very intense during bloodfeeding and epithelial and muscular cells must resist the stress, modifying the actin cytoskeleton and coordinating intracellular responses by signaling. Microorganisms present in midgut contents reproduce and interact with epithelial cells triggering innate immune response. When infectious agents are present in the blood meal they must traverse the peritrophic matrix, an envelope formed from secretion products of epithelial cells, and evade the immune system in order to reach the epithelium and continue their journey towards salivary glands, in preparation for the transmission to the new hosts. During all these processes, proteins of mosquitoes are modified in order to deal with mechanical and biological challenges, and the aim of this work is to study these changes. This article is part of a Special Issue entitled: Proteomics, mass spectrometry and peptidomics, Cancun 2013. Guest Editors: César López-Camarillo, Victoria Pando-Robles and Bronwyn Jane Barkla. [Display omitted] •Mosquito midgut is formed by a monolayer epithelium supported by muscular strands.•Dense granules, present in resting midgut cells are emptied after blood feeding.•Dense granules contents are resynthesized 12 to 24h after blood feeding.•Blood feeding modifies midgut cytoskeleton proteins during mechanical stress.•Blood feeding modifies stress and immune proteins present in the midgut.</description><identifier>ISSN: 1874-3919</identifier><identifier>EISSN: 1876-7737</identifier><identifier>DOI: 10.1016/j.jprot.2014.07.037</identifier><identifier>PMID: 25132141</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Animals ; Anopheles - metabolism ; Anopheles - parasitology ; Anopheles albimanus ; Anopheles mosquito ; Bloodfeeding ; Cytoskeleton - metabolism ; Digestive System - metabolism ; Electron microscopy ; Electrophoresis, Gel, Two-Dimensional ; Epithelial Cells - parasitology ; Female ; Host-Parasite Interactions ; Humans ; Immunity, Innate ; Insect Vectors - metabolism ; Insect Vectors - parasitology ; Mice ; Mice, Inbred BALB C ; Midgut ; Oxidative Stress ; Perithrophic matrix ; Plasmodium ; Plasmodium - metabolism ; Proteome ; Proteomics ; Serpins - chemistry ; Signal Transduction ; Spectrometry, Mass, Electrospray Ionization ; Tandem Mass Spectrometry ; Time Factors</subject><ispartof>Journal of proteomics, 2014-12, Vol.111, p.100-112</ispartof><rights>2014 Elsevier B.V.</rights><rights>Copyright © 2014 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c392t-e65986082014c22631276a79318cf7156671d011fa696d86b926103850cfec9f3</citedby><cites>FETCH-LOGICAL-c392t-e65986082014c22631276a79318cf7156671d011fa696d86b926103850cfec9f3</cites><orcidid>0000-0002-7276-7513</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.jprot.2014.07.037$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25132141$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cázares-Raga, F.E.</creatorcontrib><creatorcontrib>Chávez-Munguía, B.</creatorcontrib><creatorcontrib>González-Calixto, C.</creatorcontrib><creatorcontrib>Ochoa-Franco, A.P.</creatorcontrib><creatorcontrib>Gawinowicz, M.A.</creatorcontrib><creatorcontrib>Rodríguez, M.H.</creatorcontrib><creatorcontrib>Hernández-Hernández, F.C.</creatorcontrib><title>Morphological and proteomic characterization of midgut of the malaria vector Anopheles albimanus at early time after a blood feeding</title><title>Journal of proteomics</title><addtitle>J Proteomics</addtitle><description>The midgut of anopheline mosquito is the entry of Plasmodium, the causative agent of malaria.When the mosquito feeds on parasite infected host, Plasmodium parasites reach the midgut and must confront digestive enzymes, the innate immune response and go across the peritrophic matrix (PM), a thick extracellular sheath secreted by the mosquito midgut epithelial cells. Then, to continue its development, the parasite must reach the salivary glands to achieve transmission to a vertebrate host. We report here the morphological and biochemical descriptions of the midgut changes after a blood meal in Anopheles albimanus. Before blood feeding, midgut epithelial cells contained numerous electrondense vesicles distributed in the central to apical side. These vesicles were secreted to the luminal side of the midgut after a blood meal. At early times after blood ingest, the PM is formed near microvilli as a granulous amorphous material and after it consolidates forming a highly organized fibrillar structure, constituted by layers of electrondense and electronlucent regions. Proteomic comparative analysis of sugar and blood fed midguts showed several molecules that modify their abundance after blood intake; these include innate immunity, cytoskeletal, stress response, signaling, and digestive, detoxifying and metabolism enzymes. Biological significance In the midgut of mosquitoes during bloodfeeding, many simultaneous processes occur, including digestion, innate immune activities, cytoskeleton modifications, construction of a peritrophic matrix and hormone production, between others. Mechanical forces are very intense during bloodfeeding and epithelial and muscular cells must resist the stress, modifying the actin cytoskeleton and coordinating intracellular responses by signaling. Microorganisms present in midgut contents reproduce and interact with epithelial cells triggering innate immune response. When infectious agents are present in the blood meal they must traverse the peritrophic matrix, an envelope formed from secretion products of epithelial cells, and evade the immune system in order to reach the epithelium and continue their journey towards salivary glands, in preparation for the transmission to the new hosts. During all these processes, proteins of mosquitoes are modified in order to deal with mechanical and biological challenges, and the aim of this work is to study these changes. This article is part of a Special Issue entitled: Proteomics, mass spectrometry and peptidomics, Cancun 2013. Guest Editors: César López-Camarillo, Victoria Pando-Robles and Bronwyn Jane Barkla. 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Then, to continue its development, the parasite must reach the salivary glands to achieve transmission to a vertebrate host. We report here the morphological and biochemical descriptions of the midgut changes after a blood meal in Anopheles albimanus. Before blood feeding, midgut epithelial cells contained numerous electrondense vesicles distributed in the central to apical side. These vesicles were secreted to the luminal side of the midgut after a blood meal. At early times after blood ingest, the PM is formed near microvilli as a granulous amorphous material and after it consolidates forming a highly organized fibrillar structure, constituted by layers of electrondense and electronlucent regions. Proteomic comparative analysis of sugar and blood fed midguts showed several molecules that modify their abundance after blood intake; these include innate immunity, cytoskeletal, stress response, signaling, and digestive, detoxifying and metabolism enzymes. Biological significance In the midgut of mosquitoes during bloodfeeding, many simultaneous processes occur, including digestion, innate immune activities, cytoskeleton modifications, construction of a peritrophic matrix and hormone production, between others. Mechanical forces are very intense during bloodfeeding and epithelial and muscular cells must resist the stress, modifying the actin cytoskeleton and coordinating intracellular responses by signaling. Microorganisms present in midgut contents reproduce and interact with epithelial cells triggering innate immune response. When infectious agents are present in the blood meal they must traverse the peritrophic matrix, an envelope formed from secretion products of epithelial cells, and evade the immune system in order to reach the epithelium and continue their journey towards salivary glands, in preparation for the transmission to the new hosts. During all these processes, proteins of mosquitoes are modified in order to deal with mechanical and biological challenges, and the aim of this work is to study these changes. This article is part of a Special Issue entitled: Proteomics, mass spectrometry and peptidomics, Cancun 2013. Guest Editors: César López-Camarillo, Victoria Pando-Robles and Bronwyn Jane Barkla. [Display omitted] •Mosquito midgut is formed by a monolayer epithelium supported by muscular strands.•Dense granules, present in resting midgut cells are emptied after blood feeding.•Dense granules contents are resynthesized 12 to 24h after blood feeding.•Blood feeding modifies midgut cytoskeleton proteins during mechanical stress.•Blood feeding modifies stress and immune proteins present in the midgut.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>25132141</pmid><doi>10.1016/j.jprot.2014.07.037</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-7276-7513</orcidid></addata></record>
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subjects Animals
Anopheles - metabolism
Anopheles - parasitology
Anopheles albimanus
Anopheles mosquito
Bloodfeeding
Cytoskeleton - metabolism
Digestive System - metabolism
Electron microscopy
Electrophoresis, Gel, Two-Dimensional
Epithelial Cells - parasitology
Female
Host-Parasite Interactions
Humans
Immunity, Innate
Insect Vectors - metabolism
Insect Vectors - parasitology
Mice
Mice, Inbred BALB C
Midgut
Oxidative Stress
Perithrophic matrix
Plasmodium
Plasmodium - metabolism
Proteome
Proteomics
Serpins - chemistry
Signal Transduction
Spectrometry, Mass, Electrospray Ionization
Tandem Mass Spectrometry
Time Factors
title Morphological and proteomic characterization of midgut of the malaria vector Anopheles albimanus at early time after a blood feeding
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