{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T20:49:43Z","timestamp":1792788583500,"version":"4.5.0"},"update-to":[{"DOI":"10.1371\/journal.ppat.1009615","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,6,10]],"date-time":"2021-06-10T00:00:00Z","timestamp":1623283200000}}],"reference-count":94,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2021,5,28]],"date-time":"2021-05-28T00:00:00Z","timestamp":1622160000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000104","name":"National Aeronautics and Space Administration","doi-asserted-by":"publisher","award":["NNX15AB42G"],"award-info":[{"award-number":["NNX15AB42G"]}],"id":[{"id":"10.13039\/100000104","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["1121817"],"award-info":[{"award-number":["1121817"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["2022235"],"award-info":[{"award-number":["2022235"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["G12MD007603-30"],"award-info":[{"award-number":["G12MD007603-30"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["1F31GM111052-01A1"],"award-info":[{"award-number":["1F31GM111052-01A1"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Howard and Vicki Palefsky Fellowship"}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>\n                    The wasps\n                    <jats:italic>Leptopilina heterotoma<\/jats:italic>\n                    parasitize and ingest their\n                    <jats:italic>Drosophila<\/jats:italic>\n                    hosts. They produce extracellular vesicles (EVs) in the venom that are packed with proteins, some of which perform immune suppressive functions. EV interactions with blood cells of host larvae are linked to hematopoietic depletion, immune suppression, and parasite success. But how EVs disperse within the host, enter and kill hematopoietic cells is not well understood. Using an antibody marker for\n                    <jats:italic>L<\/jats:italic>\n                    .\n                    <jats:italic>heterotoma<\/jats:italic>\n                    EVs, we show that these parasite-derived structures are readily distributed within the hosts\u2019 hemolymphatic system. EVs converge around the tightly clustered cells of the posterior signaling center (PSC) of the larval lymph gland, a small hematopoietic organ in\n                    <jats:italic>Drosophila<\/jats:italic>\n                    . The PSC serves as a source of developmental signals in na\u00efve animals. In wasp-infected animals, the PSC directs the differentiation of lymph gland progenitors into lamellocytes. These lamellocytes are needed to encapsulate the wasp egg and block parasite development. We found that\n                    <jats:italic>L<\/jats:italic>\n                    .\n                    <jats:italic>heterotoma<\/jats:italic>\n                    infection disassembles the PSC and PSC cells disperse into the disintegrating lymph gland lobes. Genetically manipulated PSC-less lymph glands remain non-responsive and largely intact in the face of\n                    <jats:italic>L<\/jats:italic>\n                    .\n                    <jats:italic>heterotoma<\/jats:italic>\n                    infection. We also show that the larval lymph gland progenitors use the endocytic machinery to internalize EVs. Once inside,\n                    <jats:italic>L<\/jats:italic>\n                    .\n                    <jats:italic>heterotoma<\/jats:italic>\n                    EVs damage the Rab7- and LAMP-positive late endocytic and phagolysosomal compartments. Rab5 maintains hematopoietic and immune quiescence as\n                    <jats:italic>Rab5<\/jats:italic>\n                    knockdown results in hematopoietic over-proliferation and ectopic lamellocyte differentiation. Thus, both aspects of anti-parasite immunity, i.e., (a) phagocytosis of the wasp\u2019s immune-suppressive EVs, and (b) progenitor differentiation for wasp egg encapsulation reside in the lymph gland. These results help explain why the lymph gland is specifically and precisely targeted for destruction. The parasite\u2019s simultaneous and multipronged approach to block cellular immunity not only eliminates blood cells, but also tactically blocks the genetic programming needed for supplementary hematopoietic differentiation necessary for host success. In addition to its known functions in hematopoiesis, our results highlight a previously unrecognized phagocytic role of the lymph gland in cellular immunity. EV-mediated virulence strategies described for\n                    <jats:italic>L<\/jats:italic>\n                    .\n                    <jats:italic>heterotoma<\/jats:italic>\n                    are likely to be shared by other parasitoid wasps; their understanding can improve the design and development of novel therapeutics and biopesticides as well as help protect biodiversity.\n                  <\/jats:p>","DOI":"10.1371\/journal.ppat.1009615","type":"journal-article","created":{"date-parts":[[2021,5,28]],"date-time":"2021-05-28T15:58:43Z","timestamp":1622217523000},"page":"e1009615","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":19,"title":["A parasitoid wasp of Drosophila employs preemptive and reactive strategies to deplete its host\u2019s blood cells"],"prefix":"10.1371","volume":"17","author":[{"given":"Johnny R.","family":"Ramroop","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4625-4228","authenticated-orcid":true,"given":"Mary Ellen","family":"Heavner","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2507-9005","authenticated-orcid":true,"given":"Zubaidul H.","family":"Razzak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6436-639X","authenticated-orcid":true,"given":"Shubha","family":"Govind","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,5,28]]},"reference":[{"key":"ppat.1009615.ref001","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1146\/annurev.ento.54.110807.090556","article-title":"Manipulation of host behavior by 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