Molecular characterization of tsetse's proboscis and its response to Trypanosoma congolense infection

Tsetse flies (Glossina spp.) transmit parasitic African trypanosomes (Trypanosoma spp.), including Trypanosoma congolense, which causes animal African trypanosomiasis (AAT). AAT detrimentally affects agricultural activities in sub-Saharan Africa and has negative impacts on the livelihood and nutrien...

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Veröffentlicht in:PLoS neglected tropical diseases 2017-11, Vol.11 (11), p.e0006057-e0006057
Hauptverfasser: Awuoche, Erick O, Weiss, Brian L, Vigneron, Aurélien, Mireji, Paul O, Aksoy, Emre, Nyambega, Benson, Attardo, Geoffrey M, Wu, Yineng, O'Neill, Michelle, Murilla, Grace, Aksoy, Serap
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container_title PLoS neglected tropical diseases
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creator Awuoche, Erick O
Weiss, Brian L
Vigneron, Aurélien
Mireji, Paul O
Aksoy, Emre
Nyambega, Benson
Attardo, Geoffrey M
Wu, Yineng
O'Neill, Michelle
Murilla, Grace
Aksoy, Serap
description Tsetse flies (Glossina spp.) transmit parasitic African trypanosomes (Trypanosoma spp.), including Trypanosoma congolense, which causes animal African trypanosomiasis (AAT). AAT detrimentally affects agricultural activities in sub-Saharan Africa and has negative impacts on the livelihood and nutrient availability for the affected communities. After tsetse ingests an infectious blood meal, T. congolense sequentially colonizes the fly's gut and proboscis (PB) organs before being transmitted to new mammalian hosts during subsequent feedings. Despite the importance of PB in blood feeding and disease transmission, little is known about its molecular composition, function and response to trypanosome infection. To bridge this gap, we used RNA-seq analysis to determine its molecular characteristics and responses to trypanosome infection. By comparing the PB transcriptome to whole head and midgut transcriptomes, we identified 668 PB-enriched transcripts that encoded proteins associated with muscle tissue, organ development, chemosensation and chitin-cuticle structure development. Moreover, transcripts encoding putative mechanoreceptors that monitor blood flow during tsetse feeding and interact with trypanosomes were also expressed in the PB. Microscopic analysis of the PB revealed cellular structures associated with muscles and cells. Infection with T. congolense resulted in increased and decreased expression of 38 and 88 transcripts, respectively. Twelve of these differentially expressed transcripts were PB-enriched. Among the transcripts induced upon infection were those encoding putative proteins associated with cell division function(s), suggesting enhanced tissue renewal, while those suppressed were associated with metabolic processes, extracellular matrix and ATP-binding as well as immunity. These results suggest that PB is a muscular organ with chemosensory and mechanosensory capabilities. The mechanoreceptors may be point of PB-trypanosomes interactions. T. congolense infection resulted in reduced metabolic and immune capacity of the PB. The molecular knowledge on the composition and putative functions of PB forms the foundation to identify new targets to disrupt tsetse's ability to feed and parasite transmission.
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AAT detrimentally affects agricultural activities in sub-Saharan Africa and has negative impacts on the livelihood and nutrient availability for the affected communities. After tsetse ingests an infectious blood meal, T. congolense sequentially colonizes the fly's gut and proboscis (PB) organs before being transmitted to new mammalian hosts during subsequent feedings. Despite the importance of PB in blood feeding and disease transmission, little is known about its molecular composition, function and response to trypanosome infection. To bridge this gap, we used RNA-seq analysis to determine its molecular characteristics and responses to trypanosome infection. By comparing the PB transcriptome to whole head and midgut transcriptomes, we identified 668 PB-enriched transcripts that encoded proteins associated with muscle tissue, organ development, chemosensation and chitin-cuticle structure development. Moreover, transcripts encoding putative mechanoreceptors that monitor blood flow during tsetse feeding and interact with trypanosomes were also expressed in the PB. Microscopic analysis of the PB revealed cellular structures associated with muscles and cells. Infection with T. congolense resulted in increased and decreased expression of 38 and 88 transcripts, respectively. Twelve of these differentially expressed transcripts were PB-enriched. Among the transcripts induced upon infection were those encoding putative proteins associated with cell division function(s), suggesting enhanced tissue renewal, while those suppressed were associated with metabolic processes, extracellular matrix and ATP-binding as well as immunity. These results suggest that PB is a muscular organ with chemosensory and mechanosensory capabilities. The mechanoreceptors may be point of PB-trypanosomes interactions. T. congolense infection resulted in reduced metabolic and immune capacity of the PB. The molecular knowledge on the composition and putative functions of PB forms the foundation to identify new targets to disrupt tsetse's ability to feed and parasite transmission.</description><identifier>ISSN: 1935-2735</identifier><identifier>ISSN: 1935-2727</identifier><identifier>EISSN: 1935-2735</identifier><identifier>DOI: 10.1371/journal.pntd.0006057</identifier><identifier>PMID: 29155830</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>African trypanosomiasis ; Agriculture ; Animal cuticle ; Animal Structures - parasitology ; Animals ; ATP ; Biochemistry ; Biology and Life Sciences ; Biotechnology ; Blood ; Blood flow ; Body organs ; Bridges ; Capacity ; Cell division ; Cellular structure ; Chemoreception ; Chitin ; Coding ; Developmental biology ; Disease transmission ; Drosophila ; Epidemiology ; Evolution ; Extracellular ; Extracellular matrix ; Feeding ; Gene expression ; Gene Expression Profiling ; Genes ; Host-Pathogen Interactions ; Hosts ; Immunity ; Immunology ; Infections ; Insects ; Interactions ; Lectins ; Livestock ; Mechanoreceptors ; Medicine and Health Sciences ; Metabolism ; Microscopic analysis ; Midgut ; Mineral nutrients ; Muscles ; Nucleic acids ; Nutrient availability ; Organs ; Parasites ; Parasitic diseases ; Proboscis ; Proteins ; Public health ; Reactive oxygen species ; Renewal ; Ribonucleic acid ; RNA ; Sequence Analysis, RNA ; Social Sciences ; Software ; Supervision ; Target recognition ; Tissue ; Transmission ; Tropical diseases ; Trypanosoma congolense ; Trypanosoma congolense - growth &amp; development ; Trypanosome ; Trypanosomiasis ; Tsetse flies ; Tsetse Flies - parasitology ; Vector-borne diseases ; Viral infections ; Virology</subject><ispartof>PLoS neglected tropical diseases, 2017-11, Vol.11 (11), p.e0006057-e0006057</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: infection. PLoS Negl Trop Dis 11(11): e0006057. https://doi.org/10.1371/journal.pntd.0006057</rights><rights>2017 Awuoche et al 2017 Awuoche et al</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: infection. 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AAT detrimentally affects agricultural activities in sub-Saharan Africa and has negative impacts on the livelihood and nutrient availability for the affected communities. After tsetse ingests an infectious blood meal, T. congolense sequentially colonizes the fly's gut and proboscis (PB) organs before being transmitted to new mammalian hosts during subsequent feedings. Despite the importance of PB in blood feeding and disease transmission, little is known about its molecular composition, function and response to trypanosome infection. To bridge this gap, we used RNA-seq analysis to determine its molecular characteristics and responses to trypanosome infection. By comparing the PB transcriptome to whole head and midgut transcriptomes, we identified 668 PB-enriched transcripts that encoded proteins associated with muscle tissue, organ development, chemosensation and chitin-cuticle structure development. Moreover, transcripts encoding putative mechanoreceptors that monitor blood flow during tsetse feeding and interact with trypanosomes were also expressed in the PB. Microscopic analysis of the PB revealed cellular structures associated with muscles and cells. Infection with T. congolense resulted in increased and decreased expression of 38 and 88 transcripts, respectively. Twelve of these differentially expressed transcripts were PB-enriched. Among the transcripts induced upon infection were those encoding putative proteins associated with cell division function(s), suggesting enhanced tissue renewal, while those suppressed were associated with metabolic processes, extracellular matrix and ATP-binding as well as immunity. These results suggest that PB is a muscular organ with chemosensory and mechanosensory capabilities. The mechanoreceptors may be point of PB-trypanosomes interactions. T. congolense infection resulted in reduced metabolic and immune capacity of the PB. The molecular knowledge on the composition and putative functions of PB forms the foundation to identify new targets to disrupt tsetse's ability to feed and parasite transmission.</description><subject>African trypanosomiasis</subject><subject>Agriculture</subject><subject>Animal cuticle</subject><subject>Animal Structures - parasitology</subject><subject>Animals</subject><subject>ATP</subject><subject>Biochemistry</subject><subject>Biology and Life Sciences</subject><subject>Biotechnology</subject><subject>Blood</subject><subject>Blood flow</subject><subject>Body organs</subject><subject>Bridges</subject><subject>Capacity</subject><subject>Cell division</subject><subject>Cellular structure</subject><subject>Chemoreception</subject><subject>Chitin</subject><subject>Coding</subject><subject>Developmental biology</subject><subject>Disease transmission</subject><subject>Drosophila</subject><subject>Epidemiology</subject><subject>Evolution</subject><subject>Extracellular</subject><subject>Extracellular matrix</subject><subject>Feeding</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genes</subject><subject>Host-Pathogen Interactions</subject><subject>Hosts</subject><subject>Immunity</subject><subject>Immunology</subject><subject>Infections</subject><subject>Insects</subject><subject>Interactions</subject><subject>Lectins</subject><subject>Livestock</subject><subject>Mechanoreceptors</subject><subject>Medicine and Health Sciences</subject><subject>Metabolism</subject><subject>Microscopic analysis</subject><subject>Midgut</subject><subject>Mineral nutrients</subject><subject>Muscles</subject><subject>Nucleic acids</subject><subject>Nutrient availability</subject><subject>Organs</subject><subject>Parasites</subject><subject>Parasitic diseases</subject><subject>Proboscis</subject><subject>Proteins</subject><subject>Public health</subject><subject>Reactive oxygen species</subject><subject>Renewal</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Sequence Analysis, RNA</subject><subject>Social Sciences</subject><subject>Software</subject><subject>Supervision</subject><subject>Target recognition</subject><subject>Tissue</subject><subject>Transmission</subject><subject>Tropical diseases</subject><subject>Trypanosoma congolense</subject><subject>Trypanosoma congolense - growth &amp; development</subject><subject>Trypanosome</subject><subject>Trypanosomiasis</subject><subject>Tsetse flies</subject><subject>Tsetse Flies - parasitology</subject><subject>Vector-borne diseases</subject><subject>Viral infections</subject><subject>Virology</subject><issn>1935-2735</issn><issn>1935-2727</issn><issn>1935-2735</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptkl1vFCEUhidGY2v1HxidxES92RWGAYYbk6bxo0mNN_WanIEzuzSzwwhMk_rrZdxps2saIBB4znvg5RTFa0rWlEn66cZPYYB-PQ7JrgkhgnD5pDilivFVJRl_erA-KV7EeEMIV7yhz4uTSlHOG0ZOC_zhezRTD6E0WwhgEgb3B5LzQ-m7MkXM_UMsx-BbH42LJQy2dCmWAePoh4hl8uV1uBth8NHvoDR-2GTN-cQNHZpZ6mXxrIM-4qtlPit-ff1yffF9dfXz2-XF-dXKiKpOK9rYTjGCXV3XlRAVkUbm0bYta9FUrDFUSN5ZpAJqSlpsrCGiQjTMNAY7dla83euOvY96cShqqqQUXAlVZ-JyT1gPN3oMbgfhTntw-t-GDxsNITnTo26R1xZAGWJNTZq6IVa2lQQLwrQEeNb6vGSb2h1ag0MK0B-JHp8Mbqs3_lZzobiULAt8XASC_z1hTHrnosG-hwH9NN9bCKVqTlRG3_2HPv66hdpAfkC23-e8ZhbV5zx7l-VYk6n1I1RuFncufx92Lu8fBbw_CNgi9GkbfT_NXxuPwXoPmuBjDNg9mEGJnqv2_tZ6rlq9VG0Oe3No5EPQfZmyv6Dj7Es</recordid><startdate>20171120</startdate><enddate>20171120</enddate><creator>Awuoche, Erick O</creator><creator>Weiss, Brian L</creator><creator>Vigneron, Aurélien</creator><creator>Mireji, Paul O</creator><creator>Aksoy, Emre</creator><creator>Nyambega, Benson</creator><creator>Attardo, Geoffrey M</creator><creator>Wu, Yineng</creator><creator>O'Neill, Michelle</creator><creator>Murilla, Grace</creator><creator>Aksoy, Serap</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7SS</scope><scope>7T2</scope><scope>7T7</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8C1</scope><scope>8FD</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>F1W</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>K9.</scope><scope>L.G</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-1330-8296</orcidid></search><sort><creationdate>20171120</creationdate><title>Molecular characterization of tsetse's proboscis and its response to Trypanosoma congolense infection</title><author>Awuoche, Erick O ; Weiss, Brian L ; Vigneron, Aurélien ; Mireji, Paul O ; Aksoy, Emre ; Nyambega, Benson ; Attardo, Geoffrey M ; Wu, Yineng ; O'Neill, Michelle ; Murilla, Grace ; Aksoy, Serap</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c624t-18df930ef444266207c707cbbb3bec238c1675fde16a410be8dc062eec3c8cef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>African trypanosomiasis</topic><topic>Agriculture</topic><topic>Animal cuticle</topic><topic>Animal Structures - parasitology</topic><topic>Animals</topic><topic>ATP</topic><topic>Biochemistry</topic><topic>Biology and Life Sciences</topic><topic>Biotechnology</topic><topic>Blood</topic><topic>Blood flow</topic><topic>Body organs</topic><topic>Bridges</topic><topic>Capacity</topic><topic>Cell division</topic><topic>Cellular structure</topic><topic>Chemoreception</topic><topic>Chitin</topic><topic>Coding</topic><topic>Developmental biology</topic><topic>Disease transmission</topic><topic>Drosophila</topic><topic>Epidemiology</topic><topic>Evolution</topic><topic>Extracellular</topic><topic>Extracellular matrix</topic><topic>Feeding</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Genes</topic><topic>Host-Pathogen Interactions</topic><topic>Hosts</topic><topic>Immunity</topic><topic>Immunology</topic><topic>Infections</topic><topic>Insects</topic><topic>Interactions</topic><topic>Lectins</topic><topic>Livestock</topic><topic>Mechanoreceptors</topic><topic>Medicine and Health Sciences</topic><topic>Metabolism</topic><topic>Microscopic analysis</topic><topic>Midgut</topic><topic>Mineral nutrients</topic><topic>Muscles</topic><topic>Nucleic acids</topic><topic>Nutrient availability</topic><topic>Organs</topic><topic>Parasites</topic><topic>Parasitic diseases</topic><topic>Proboscis</topic><topic>Proteins</topic><topic>Public health</topic><topic>Reactive oxygen species</topic><topic>Renewal</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Sequence Analysis, RNA</topic><topic>Social Sciences</topic><topic>Software</topic><topic>Supervision</topic><topic>Target recognition</topic><topic>Tissue</topic><topic>Transmission</topic><topic>Tropical diseases</topic><topic>Trypanosoma congolense</topic><topic>Trypanosoma congolense - growth &amp; 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AAT detrimentally affects agricultural activities in sub-Saharan Africa and has negative impacts on the livelihood and nutrient availability for the affected communities. After tsetse ingests an infectious blood meal, T. congolense sequentially colonizes the fly's gut and proboscis (PB) organs before being transmitted to new mammalian hosts during subsequent feedings. Despite the importance of PB in blood feeding and disease transmission, little is known about its molecular composition, function and response to trypanosome infection. To bridge this gap, we used RNA-seq analysis to determine its molecular characteristics and responses to trypanosome infection. By comparing the PB transcriptome to whole head and midgut transcriptomes, we identified 668 PB-enriched transcripts that encoded proteins associated with muscle tissue, organ development, chemosensation and chitin-cuticle structure development. Moreover, transcripts encoding putative mechanoreceptors that monitor blood flow during tsetse feeding and interact with trypanosomes were also expressed in the PB. Microscopic analysis of the PB revealed cellular structures associated with muscles and cells. Infection with T. congolense resulted in increased and decreased expression of 38 and 88 transcripts, respectively. Twelve of these differentially expressed transcripts were PB-enriched. Among the transcripts induced upon infection were those encoding putative proteins associated with cell division function(s), suggesting enhanced tissue renewal, while those suppressed were associated with metabolic processes, extracellular matrix and ATP-binding as well as immunity. These results suggest that PB is a muscular organ with chemosensory and mechanosensory capabilities. The mechanoreceptors may be point of PB-trypanosomes interactions. T. congolense infection resulted in reduced metabolic and immune capacity of the PB. The molecular knowledge on the composition and putative functions of PB forms the foundation to identify new targets to disrupt tsetse's ability to feed and parasite transmission.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29155830</pmid><doi>10.1371/journal.pntd.0006057</doi><orcidid>https://orcid.org/0000-0002-1330-8296</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1935-2735
ispartof PLoS neglected tropical diseases, 2017-11, Vol.11 (11), p.e0006057-e0006057
issn 1935-2735
1935-2727
1935-2735
language eng
recordid cdi_plos_journals_1977659694
source Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; PubMed Central Open Access
subjects African trypanosomiasis
Agriculture
Animal cuticle
Animal Structures - parasitology
Animals
ATP
Biochemistry
Biology and Life Sciences
Biotechnology
Blood
Blood flow
Body organs
Bridges
Capacity
Cell division
Cellular structure
Chemoreception
Chitin
Coding
Developmental biology
Disease transmission
Drosophila
Epidemiology
Evolution
Extracellular
Extracellular matrix
Feeding
Gene expression
Gene Expression Profiling
Genes
Host-Pathogen Interactions
Hosts
Immunity
Immunology
Infections
Insects
Interactions
Lectins
Livestock
Mechanoreceptors
Medicine and Health Sciences
Metabolism
Microscopic analysis
Midgut
Mineral nutrients
Muscles
Nucleic acids
Nutrient availability
Organs
Parasites
Parasitic diseases
Proboscis
Proteins
Public health
Reactive oxygen species
Renewal
Ribonucleic acid
RNA
Sequence Analysis, RNA
Social Sciences
Software
Supervision
Target recognition
Tissue
Transmission
Tropical diseases
Trypanosoma congolense
Trypanosoma congolense - growth & development
Trypanosome
Trypanosomiasis
Tsetse flies
Tsetse Flies - parasitology
Vector-borne diseases
Viral infections
Virology
title Molecular characterization of tsetse's proboscis and its response to Trypanosoma congolense infection
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