Novel Babesia bovis exported proteins that modify properties of infected red blood cells
Babesia bovis causes a pathogenic form of babesiosis in cattle. Following invasion of red blood cells (RBCs) the parasite extensively modifies host cell structural and mechanical properties via the export of numerous proteins. Despite their crucial role in virulence and pathogenesis, such proteins h...
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| creator | Hakimi, Hassan Templeton, Thomas J Sakaguchi, Miako Yamagishi, Junya Miyazaki, Shinya Yahata, Kazuhide Uchihashi, Takayuki Kawazu, Shin-Ichiro Kaneko, Osamu Asada, Masahito |
| description | Babesia bovis causes a pathogenic form of babesiosis in cattle. Following invasion of red blood cells (RBCs) the parasite extensively modifies host cell structural and mechanical properties via the export of numerous proteins. Despite their crucial role in virulence and pathogenesis, such proteins have not been comprehensively characterized in B. bovis. Here we describe the surface biotinylation of infected RBCs (iRBCs), followed by proteomic analysis. We describe a multigene family (mtm) that encodes predicted multi-transmembrane integral membrane proteins which are exported and expressed on the surface of iRBCs. One mtm gene was downregulated in blasticidin-S (BS) resistant parasites, suggesting an association with BS uptake. Induced knockdown of a novel exported protein encoded by BBOV_III004280, named VESA export-associated protein (BbVEAP), resulted in a decreased growth rate, reduced RBC surface ridge numbers, mis-localized VESA1, and abrogated cytoadhesion to endothelial cells, suggesting that BbVEAP is a novel virulence factor for B. bovis. |
| doi_str_mv | 10.1371/journal.ppat.1008917 |
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Following invasion of red blood cells (RBCs) the parasite extensively modifies host cell structural and mechanical properties via the export of numerous proteins. Despite their crucial role in virulence and pathogenesis, such proteins have not been comprehensively characterized in B. bovis. Here we describe the surface biotinylation of infected RBCs (iRBCs), followed by proteomic analysis. We describe a multigene family (mtm) that encodes predicted multi-transmembrane integral membrane proteins which are exported and expressed on the surface of iRBCs. One mtm gene was downregulated in blasticidin-S (BS) resistant parasites, suggesting an association with BS uptake. Induced knockdown of a novel exported protein encoded by BBOV_III004280, named VESA export-associated protein (BbVEAP), resulted in a decreased growth rate, reduced RBC surface ridge numbers, mis-localized VESA1, and abrogated cytoadhesion to endothelial cells, suggesting that BbVEAP is a novel virulence factor for B. bovis.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1008917</identifier><identifier>PMID: 33017449</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Babesia ; Babesia bovis ; Babesia bovis - genetics ; Babesia bovis - pathogenicity ; Babesiosis ; Babesiosis - parasitology ; Biology and Life Sciences ; Biotinylation ; Blood ; Blood cells ; Brain research ; Cattle ; Cattle Diseases - parasitology ; Cell interaction ; Cellular proteins ; Chromatography ; Collaboration ; Cytoplasm ; Endothelial cells ; Endothelial Cells - parasitology ; Erythrocytes ; Erythrocytes - parasitology ; Exports ; Funding ; Genetic aspects ; Growth rate ; Health aspects ; Integral membrane proteins ; Mass spectrometry ; Mechanical properties ; Medicine and Health Sciences ; Membrane Proteins ; Parasite resistance ; Parasites ; Parasites - pathogenicity ; Parasitic diseases ; Pathogenesis ; Peptides ; Protein transport ; Proteins ; Proteomics - methods ; Research and Analysis Methods ; Scientific imaging ; Veterinary medicine ; Virulence ; Virulence (Microbiology) ; Virulence factors ; Virulence Factors - genetics ; Zoonoses</subject><ispartof>PLoS pathogens, 2020-10, Vol.16 (10), p.e1008917-e1008917</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Hakimi 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>2020 Hakimi et al 2020 Hakimi et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c771t-e1bcb4a6be7e373dee0c233e541dfe8f0ef3302ae5f2e2aa7ad30e3397eddb0b3</citedby><cites>FETCH-LOGICAL-c771t-e1bcb4a6be7e373dee0c233e541dfe8f0ef3302ae5f2e2aa7ad30e3397eddb0b3</cites><orcidid>0000-0003-4780-8878 ; 0000-0001-5105-3100 ; 0000-0003-0042-6856 ; 0000-0003-0675-8296 ; 0000-0003-4326-4025 ; 0000-0002-0263-5312 ; 0000-0001-6678-7393</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/PMC7561165/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7561165/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33017449$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hakimi, Hassan</creatorcontrib><creatorcontrib>Templeton, Thomas J</creatorcontrib><creatorcontrib>Sakaguchi, Miako</creatorcontrib><creatorcontrib>Yamagishi, Junya</creatorcontrib><creatorcontrib>Miyazaki, Shinya</creatorcontrib><creatorcontrib>Yahata, Kazuhide</creatorcontrib><creatorcontrib>Uchihashi, Takayuki</creatorcontrib><creatorcontrib>Kawazu, Shin-Ichiro</creatorcontrib><creatorcontrib>Kaneko, Osamu</creatorcontrib><creatorcontrib>Asada, Masahito</creatorcontrib><title>Novel Babesia bovis exported proteins that modify properties of infected red blood cells</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Babesia bovis causes a pathogenic form of babesiosis in cattle. Following invasion of red blood cells (RBCs) the parasite extensively modifies host cell structural and mechanical properties via the export of numerous proteins. Despite their crucial role in virulence and pathogenesis, such proteins have not been comprehensively characterized in B. bovis. Here we describe the surface biotinylation of infected RBCs (iRBCs), followed by proteomic analysis. We describe a multigene family (mtm) that encodes predicted multi-transmembrane integral membrane proteins which are exported and expressed on the surface of iRBCs. One mtm gene was downregulated in blasticidin-S (BS) resistant parasites, suggesting an association with BS uptake. 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Following invasion of red blood cells (RBCs) the parasite extensively modifies host cell structural and mechanical properties via the export of numerous proteins. Despite their crucial role in virulence and pathogenesis, such proteins have not been comprehensively characterized in B. bovis. Here we describe the surface biotinylation of infected RBCs (iRBCs), followed by proteomic analysis. We describe a multigene family (mtm) that encodes predicted multi-transmembrane integral membrane proteins which are exported and expressed on the surface of iRBCs. One mtm gene was downregulated in blasticidin-S (BS) resistant parasites, suggesting an association with BS uptake. Induced knockdown of a novel exported protein encoded by BBOV_III004280, named VESA export-associated protein (BbVEAP), resulted in a decreased growth rate, reduced RBC surface ridge numbers, mis-localized VESA1, and abrogated cytoadhesion to endothelial cells, suggesting that BbVEAP is a novel virulence factor for B. bovis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33017449</pmid><doi>10.1371/journal.ppat.1008917</doi><orcidid>https://orcid.org/0000-0003-4780-8878</orcidid><orcidid>https://orcid.org/0000-0001-5105-3100</orcidid><orcidid>https://orcid.org/0000-0003-0042-6856</orcidid><orcidid>https://orcid.org/0000-0003-0675-8296</orcidid><orcidid>https://orcid.org/0000-0003-4326-4025</orcidid><orcidid>https://orcid.org/0000-0002-0263-5312</orcidid><orcidid>https://orcid.org/0000-0001-6678-7393</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Babesia Babesia bovis Babesia bovis - genetics Babesia bovis - pathogenicity Babesiosis Babesiosis - parasitology Biology and Life Sciences Biotinylation Blood Blood cells Brain research Cattle Cattle Diseases - parasitology Cell interaction Cellular proteins Chromatography Collaboration Cytoplasm Endothelial cells Endothelial Cells - parasitology Erythrocytes Erythrocytes - parasitology Exports Funding Genetic aspects Growth rate Health aspects Integral membrane proteins Mass spectrometry Mechanical properties Medicine and Health Sciences Membrane Proteins Parasite resistance Parasites Parasites - pathogenicity Parasitic diseases Pathogenesis Peptides Protein transport Proteins Proteomics - methods Research and Analysis Methods Scientific imaging Veterinary medicine Virulence Virulence (Microbiology) Virulence factors Virulence Factors - genetics Zoonoses |
| title | Novel Babesia bovis exported proteins that modify properties of infected red blood cells |
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