Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses
IntroductionBlood-feeding arthropods rely on robust cellular and humoral immunity to control pathogen invasion and replication. Tick hemocytes produce factors that can facilitate or suppress microbial infection and pathogenesis. Despite the importance of hemocytes in regulating microbial infection,...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1094326/full |
| _version_ | 1811167215258435584 |
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| author | Abdulsalam Adegoke Jose M. C. Ribeiro Sidney Brown Ryan C. Smith Shahid Karim |
| author_facet | Abdulsalam Adegoke Jose M. C. Ribeiro Sidney Brown Ryan C. Smith Shahid Karim |
| author_sort | Abdulsalam Adegoke |
| collection | DOAJ |
| description | IntroductionBlood-feeding arthropods rely on robust cellular and humoral immunity to control pathogen invasion and replication. Tick hemocytes produce factors that can facilitate or suppress microbial infection and pathogenesis. Despite the importance of hemocytes in regulating microbial infection, understanding of their basic biology and molecular mechanisms remains limited.MethodsHere we combined histomorphology and functional analysis to identify five distinct phagocytic and non-phagocytic hemocyte populations circulating within the Gulf Coast tick Amblyomma maculatum.Results and discussionDepletion of phagocytic hemocytes using clodronate liposomes revealed their function in eliminating bacterial infection. We provide the first direct evidence that an intracellular tick-borne pathogen, Rickettsia parkeri, infects phagocytic hemocytes in Am. maculatum to modify tick cellular immune responses. A hemocyte-specific RNA-seq dataset generated from hemocytes isolated from uninfected and R. parkeri-infected partially blood-fed ticks generated ~40,000 differentially regulated transcripts, >11,000 of which were immune genes. Silencing two differentially regulated phagocytic immune marker genes (nimrod B2 and eater-two Drosophila homologs), significantly reduced hemocyte phagocytosis.ConclusionTogether, these findings represent a significant step forward in understanding how hemocytes regulate microbial homeostasis and vector competence. |
| first_indexed | 2024-04-10T16:05:28Z |
| format | Article |
| id | doaj.art-02c1552e782b424db71613fb861b91d7 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-10T16:05:28Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-02c1552e782b424db71613fb861b91d72023-02-10T05:05:22ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-02-011410.3389/fimmu.2023.10943261094326Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responsesAbdulsalam Adegoke0Jose M. C. Ribeiro1Sidney Brown2Ryan C. Smith3Shahid Karim4School of Biological, Environmental, and Earth Sciences, The University of Southern Mississippi, Hattiesburg, MS, United StatesVector Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, United StatesSchool of Biological, Environmental, and Earth Sciences, The University of Southern Mississippi, Hattiesburg, MS, United StatesDepartment of Plant Pathology, Entomology, and Microbiology, Iowa State University, Ames, IA, United StatesSchool of Biological, Environmental, and Earth Sciences, The University of Southern Mississippi, Hattiesburg, MS, United StatesIntroductionBlood-feeding arthropods rely on robust cellular and humoral immunity to control pathogen invasion and replication. Tick hemocytes produce factors that can facilitate or suppress microbial infection and pathogenesis. Despite the importance of hemocytes in regulating microbial infection, understanding of their basic biology and molecular mechanisms remains limited.MethodsHere we combined histomorphology and functional analysis to identify five distinct phagocytic and non-phagocytic hemocyte populations circulating within the Gulf Coast tick Amblyomma maculatum.Results and discussionDepletion of phagocytic hemocytes using clodronate liposomes revealed their function in eliminating bacterial infection. We provide the first direct evidence that an intracellular tick-borne pathogen, Rickettsia parkeri, infects phagocytic hemocytes in Am. maculatum to modify tick cellular immune responses. A hemocyte-specific RNA-seq dataset generated from hemocytes isolated from uninfected and R. parkeri-infected partially blood-fed ticks generated ~40,000 differentially regulated transcripts, >11,000 of which were immune genes. Silencing two differentially regulated phagocytic immune marker genes (nimrod B2 and eater-two Drosophila homologs), significantly reduced hemocyte phagocytosis.ConclusionTogether, these findings represent a significant step forward in understanding how hemocytes regulate microbial homeostasis and vector competence.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1094326/fullHemocytesclodronate liposomephagocyteRickettsia parkeritranscriptomenimrod B2 |
| spellingShingle | Abdulsalam Adegoke Jose M. C. Ribeiro Sidney Brown Ryan C. Smith Shahid Karim Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses Frontiers in Immunology Hemocytes clodronate liposome phagocyte Rickettsia parkeri transcriptome nimrod B2 |
| title | Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses |
| title_full | Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses |
| title_fullStr | Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses |
| title_full_unstemmed | Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses |
| title_short | Rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses |
| title_sort | rickettsia parkeri hijacks tick hemocytes to manipulate cellular and humoral transcriptional responses |
| topic | Hemocytes clodronate liposome phagocyte Rickettsia parkeri transcriptome nimrod B2 |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1094326/full |
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