A multi-omics approach for understanding blood digestion dynamics in Ixodes scapularis and identification of anti-tick vaccine targets
Ixodes scapularis, the black-legged tick, is a major arthropod vector that transmits the causative agents of Lyme disease and several other pathogens of human significance. The tick midgut is the main tissue involved in blood acquisition and digestion and the first organ to have contact with pathoge...
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| Format: | Article |
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Elsevier
2024-11-01
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| Series: | Ticks and Tick-Borne Diseases |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1877959X24000724 |
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| author | Jeremiah B. Reyes Molly McVicar Saransh Beniwal Arvind Sharma Richard Tillett Juli Petereit Andrew Nuss Monika Gulia-Nuss |
| author_facet | Jeremiah B. Reyes Molly McVicar Saransh Beniwal Arvind Sharma Richard Tillett Juli Petereit Andrew Nuss Monika Gulia-Nuss |
| author_sort | Jeremiah B. Reyes |
| collection | DOAJ |
| description | Ixodes scapularis, the black-legged tick, is a major arthropod vector that transmits the causative agents of Lyme disease and several other pathogens of human significance. The tick midgut is the main tissue involved in blood acquisition and digestion and the first organ to have contact with pathogens ingested through the blood meal. Gene expression in the midgut before, during, and after a blood meal may vary in response to the physiological changes due to blood feeding. A systems biology approach based on RNA and protein sequencing was used to gain insight into the changes in tick midgut transcripts and proteins during blood ingestion (unfed and partially fed) and digestion (1-, 2-, 7-, and 14 days post detachment from the host) by the Ixodes scapularis female ticks. A total of 2,726 differentially expressed transcripts, and 449 proteins were identified across the time points. Genes involved in detoxification of xenobiotics, proteases, protease inhibitors, metabolism, and immunity were differentially expressed in response to blood feeding. Similarly, proteins corresponding to the same groups were also differentially expressed. Nine genes from major gene categories were chosen as potential vaccine candidates, and, using RNA interference, the effect of these gene knockdowns on tick biology was investigated. Knockdown of these genes had variable negative impacts on tick physiology, such as the inability to engorge fully and to produce eggs and increased mortality. These and additional gene targets provide opportunities to explore novel tick control strategies. |
| format | Article |
| id | doaj-art-0dbeceaff5374b029e435da8b378b4d2 |
| institution | OA Journals |
| issn | 1877-9603 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ticks and Tick-Borne Diseases |
| spelling | doaj-art-0dbeceaff5374b029e435da8b378b4d22025-08-20T02:37:39ZengElsevierTicks and Tick-Borne Diseases1877-96032024-11-0115610237910.1016/j.ttbdis.2024.102379A multi-omics approach for understanding blood digestion dynamics in Ixodes scapularis and identification of anti-tick vaccine targetsJeremiah B. Reyes0Molly McVicar1Saransh Beniwal2Arvind Sharma3Richard Tillett4Juli Petereit5Andrew Nuss6Monika Gulia-Nuss7Department of Biochemistry and Molecular Biology, University of Nevada, Reno, USA, 89557; Nevada Bioinformatics Center, University of Nevada Reno, USA, 89557Department of Biochemistry and Molecular Biology, University of Nevada, Reno, USA, 89557Department of Biochemistry and Molecular Biology, University of Nevada, Reno, USA, 89557; Department of Computer Science and Engineering, University of Nevada, Reno, USA, 89557Department of Biochemistry and Molecular Biology, University of Nevada, Reno, USA, 89557Nevada Bioinformatics Center, University of Nevada Reno, USA, 89557Nevada Bioinformatics Center, University of Nevada Reno, USA, 89557Department of Biochemistry and Molecular Biology, University of Nevada, Reno, USA, 89557; Department of Agriculture, Veterinary, and Rangeland Science, University of Nevada Reno, USA, 89557Department of Biochemistry and Molecular Biology, University of Nevada, Reno, USA, 89557; Corresponding author.Ixodes scapularis, the black-legged tick, is a major arthropod vector that transmits the causative agents of Lyme disease and several other pathogens of human significance. The tick midgut is the main tissue involved in blood acquisition and digestion and the first organ to have contact with pathogens ingested through the blood meal. Gene expression in the midgut before, during, and after a blood meal may vary in response to the physiological changes due to blood feeding. A systems biology approach based on RNA and protein sequencing was used to gain insight into the changes in tick midgut transcripts and proteins during blood ingestion (unfed and partially fed) and digestion (1-, 2-, 7-, and 14 days post detachment from the host) by the Ixodes scapularis female ticks. A total of 2,726 differentially expressed transcripts, and 449 proteins were identified across the time points. Genes involved in detoxification of xenobiotics, proteases, protease inhibitors, metabolism, and immunity were differentially expressed in response to blood feeding. Similarly, proteins corresponding to the same groups were also differentially expressed. Nine genes from major gene categories were chosen as potential vaccine candidates, and, using RNA interference, the effect of these gene knockdowns on tick biology was investigated. Knockdown of these genes had variable negative impacts on tick physiology, such as the inability to engorge fully and to produce eggs and increased mortality. These and additional gene targets provide opportunities to explore novel tick control strategies.http://www.sciencedirect.com/science/article/pii/S1877959X24000724IxodidIxodes scapularisTranscriptomeProteomicsAnti-tick vaccineMidgut |
| spellingShingle | Jeremiah B. Reyes Molly McVicar Saransh Beniwal Arvind Sharma Richard Tillett Juli Petereit Andrew Nuss Monika Gulia-Nuss A multi-omics approach for understanding blood digestion dynamics in Ixodes scapularis and identification of anti-tick vaccine targets Ticks and Tick-Borne Diseases Ixodid Ixodes scapularis Transcriptome Proteomics Anti-tick vaccine Midgut |
| title | A multi-omics approach for understanding blood digestion dynamics in Ixodes scapularis and identification of anti-tick vaccine targets |
| title_full | A multi-omics approach for understanding blood digestion dynamics in Ixodes scapularis and identification of anti-tick vaccine targets |
| title_fullStr | A multi-omics approach for understanding blood digestion dynamics in Ixodes scapularis and identification of anti-tick vaccine targets |
| title_full_unstemmed | A multi-omics approach for understanding blood digestion dynamics in Ixodes scapularis and identification of anti-tick vaccine targets |
| title_short | A multi-omics approach for understanding blood digestion dynamics in Ixodes scapularis and identification of anti-tick vaccine targets |
| title_sort | multi omics approach for understanding blood digestion dynamics in ixodes scapularis and identification of anti tick vaccine targets |
| topic | Ixodid Ixodes scapularis Transcriptome Proteomics Anti-tick vaccine Midgut |
| url | http://www.sciencedirect.com/science/article/pii/S1877959X24000724 |
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