Theileria annulata infects B-cells in sheep, which display lower dissemination potential compared to T. lestoquardi-infected ovine B-cells

IF 3.1 2区医学 Q2 INFECTIOUS DISEASES

Ticks and Tick-borne Diseases Pub Date : 2025-01-30 DOI:10.1016/j.ttbdis.2025.102443

Shahin Tajeri , Perle Latré de Laté , Johanneke D. Hemmink , Christina Vrettou , Gordon Langsley , W. Ivan Morrison

{"title":"Theileria annulata infects B-cells in sheep, which display lower dissemination potential compared to T. lestoquardi-infected ovine B-cells","authors":"Shahin Tajeri , Perle Latré de Laté , Johanneke D. Hemmink , Christina Vrettou , Gordon Langsley , W. Ivan Morrison","doi":"10.1016/j.ttbdis.2025.102443","DOIUrl":null,"url":null,"abstract":"<div><div>Theileria annulata and Theileria lestoquardi are deadly tick-borne parasites of cattle and sheep, respectively. These parasites are transmitted by Hyalomma ticks, and their geographical distributions partially overlap, with T. annulata having a wider range. Theileria lestoquardi infection is highly pathogenic in its natural sheep and goat hosts while T. annulata infection usually causes a mild disease in these species. Interestingly, T. annulata does not produce merozoites/piroplasms in sheep and goats, therefore it is not tick-transmissible. The aim of the current study was to understand the basis of the attenuated pathogenicity of ovine infections by T. annulata. Theileria annulata and T. lestoquardi sporozoites were used to infect sheep and parasitized ovine leukocytes were isolated and phenotyped. This revealed that T. annulata sporozites target ovine B-cells, whereas T. lestoquardi sporozoite infection was not restricted to ovine B-cells. The ability of ovine B-cells infected with T. lestoquardi or T. annulata to traverse Matrigel in vitro was investigated, as a surrogate for their ability to disseminate in vivo and cause disease. The Matrigel traversal index of T. lestoquardi-transformed ovine B-cells was significantly higher than that of T. annulata-transformed ovine B-cells isolated from the same host, consistent with the reported diminished pathogenicity of T. annulata infections in sheep. Theileria lestoquardi-transformed ovine B-cells preferentially expressed matrix metalloproteinase 2 (mmp2), whereas T. annulata-infected ovine B-cells strongly expressed mmp9. Correspondingly, MMP9 protein levels and collagenase activity were higher in T. annulata-transformed ovine B-cells. However, T. annulata-transformed ovine B-cells expressed higher levels of transcripts for Tissue Inhibitor of Metallopeptidases 1 and 2 (TIMP1 and TIMP2). TIMPs are the natural endogenous inhibitors of MMPs. This argues that their heightened expression could underpin the significantly lower Matrigel traversal activity of T. annulata-infected compared to T. lestoquardi-infected ovine B-cells.</div></div>","PeriodicalId":49320,"journal":{"name":"Ticks and Tick-borne Diseases","volume":"16 2","pages":"Article 102443"},"PeriodicalIF":3.1000,"publicationDate":"2025-01-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Ticks and Tick-borne Diseases","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1877959X2500007X","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}

引用次数: 0

Abstract

Theileria annulata and Theileria lestoquardi are deadly tick-borne parasites of cattle and sheep, respectively. These parasites are transmitted by Hyalomma ticks, and their geographical distributions partially overlap, with T. annulata having a wider range. Theileria lestoquardi infection is highly pathogenic in its natural sheep and goat hosts while T. annulata infection usually causes a mild disease in these species. Interestingly, T. annulata does not produce merozoites/piroplasms in sheep and goats, therefore it is not tick-transmissible. The aim of the current study was to understand the basis of the attenuated pathogenicity of ovine infections by T. annulata. Theileria annulata and T. lestoquardi sporozoites were used to infect sheep and parasitized ovine leukocytes were isolated and phenotyped. This revealed that T. annulata sporozites target ovine B-cells, whereas T. lestoquardi sporozoite infection was not restricted to ovine B-cells. The ability of ovine B-cells infected with T. lestoquardi or T. annulata to traverse Matrigel in vitro was investigated, as a surrogate for their ability to disseminate in vivo and cause disease. The Matrigel traversal index of T. lestoquardi-transformed ovine B-cells was significantly higher than that of T. annulata-transformed ovine B-cells isolated from the same host, consistent with the reported diminished pathogenicity of T. annulata infections in sheep. Theileria lestoquardi-transformed ovine B-cells preferentially expressed matrix metalloproteinase 2 (mmp2), whereas T. annulata-infected ovine B-cells strongly expressed mmp9. Correspondingly, MMP9 protein levels and collagenase activity were higher in T. annulata-transformed ovine B-cells. However, T. annulata-transformed ovine B-cells expressed higher levels of transcripts for Tissue Inhibitor of Metallopeptidases 1 and 2 (TIMP1 and TIMP2). TIMPs are the natural endogenous inhibitors of MMPs. This argues that their heightened expression could underpin the significantly lower Matrigel traversal activity of T. annulata-infected compared to T. lestoquardi-infected ovine B-cells.

查看原文本刊更多论文

环状沙雷氏菌感染了绵羊的 B 细胞，与感染 T. lestoquardi 的绵羊 B 细胞相比，环状沙雷氏菌的传播潜力较低。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Ticks and Tick-borne Diseases INFECTIOUS DISEASES-MICROBIOLOGY

CiteScore

6.90

自引率

12.50%

发文量

185

审稿时长

6-12 weeks

期刊介绍： Ticks and Tick-borne Diseases is an international, peer-reviewed scientific journal. It publishes original research papers, short communications, state-of-the-art mini-reviews, letters to the editor, clinical-case studies, announcements of pertinent international meetings, and editorials. The journal covers a broad spectrum and brings together various disciplines, for example, zoology, microbiology, molecular biology, genetics, mathematical modelling, veterinary and human medicine. Multidisciplinary approaches and the use of conventional and novel methods/methodologies (in the field and in the laboratory) are crucial for deeper understanding of the natural processes and human behaviour/activities that result in human or animal diseases and in economic effects of ticks and tick-borne pathogens. Such understanding is essential for management of tick populations and tick-borne diseases in an effective and environmentally acceptable manner.