Hakimi Hassan, Yamagishi Junya, Sakaguchi Miako, Fathi Atefeh, Lee Jae Seung, Verocai Guilherme G, Kawazu Shin-Ichiro, Asada Masahito
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, Japan.
Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, United States of America.
PLoS Pathog. 2025 Apr 28;21(4):e1012583. doi: 10.1371/journal.ppat.1012583. eCollection 2025 Apr.
Babesia bovis causes the most pathogenic form of babesiosis in cattle, resulting in high mortality in naive adults. This parasite invades red blood cells (RBCs) within the bovine hosts where they multiply and produce clinical disease. Babesia bovis exports numerous proteins into invaded RBCs changing its properties. Thus, the infected RBCs (iRBCs) are capable to cytoadhere in the microvasculature of internal organs and brain, leading to respiratory distress, neurologic signs, and mortality. Variant Erythrocyte Surface Antigen 1 (VESA1) is one of those exported proteins by B. bovis which represents a major virulence factor due to its central role in immune evasion by antigenic variation and intravascular parasite sequestration. VESA1 is a heterodimer protein encoded by ves1α and ves1β multigene family and localized on the ridges, the focal point for cytoadhesion. To gain further insights into the molecular mechanisms of cytoadhesion of B. bovis, we panned the parasites with bovine brain microvasculature endothelial cells, which resulted in obtaining several clones with different cytoadherence abilities. The transcriptome analysis of 2 high and 2 low cytoadherent clones revealed that ves1α sequences were diversified, likely resulting from genomic recombination. On the other hand, ves1β sequences were almost identical among these 4 clones. Insertion and expression of ves1α of a clone with high binding into ef-1α locus of a low binding clone increased cytoadherence confirming the role of ves1α suggested by our transcriptome data. Whole genome sequencing of cytoadherent clones revealed active locus of ves1 on chromosome 2. These results suggest that VESA1a proteins encoded by ves1α genes determine the cytoadherence strength of B. bovis and they are in the active site for recombination.
牛巴贝斯虫引发牛最具致病性的巴贝斯虫病形式,导致初染成年牛的高死亡率。这种寄生虫侵入牛宿主内的红细胞(RBCs),在其中繁殖并引发临床疾病。牛巴贝斯虫向被侵入的红细胞输出多种蛋白质,改变其特性。因此,受感染的红细胞(iRBCs)能够在内部器官和大脑的微血管中发生细胞黏附,导致呼吸窘迫、神经症状和死亡。变异红细胞表面抗原1(VESA1)是牛巴贝斯虫输出的此类蛋白质之一,由于其在通过抗原变异和血管内寄生虫滞留进行免疫逃避中发挥核心作用,它是一种主要的毒力因子。VESA1是一种异二聚体蛋白,由ves1α和ves1β多基因家族编码,定位于嵴上,即细胞黏附的焦点。为了进一步深入了解牛巴贝斯虫细胞黏附的分子机制,我们用牛脑微血管内皮细胞淘选寄生虫,从而获得了几个具有不同细胞黏附能力的克隆。对2个高细胞黏附克隆和2个低细胞黏附克隆的转录组分析表明,ves1α序列是多样化的,可能是基因组重组的结果。另一方面,在这4个克隆中,ves1β序列几乎相同。将一个高结合力克隆的ves1α插入并表达于一个低结合力克隆的ef - 1α位点,增加了细胞黏附,证实了我们转录组数据所提示的ves1α的作用。细胞黏附克隆的全基因组测序揭示了2号染色体上ves1的活性位点。这些结果表明,由ves1α基因编码的VESA1a蛋白决定了牛巴贝斯虫的细胞黏附强度,并且它们处于重组的活性位点。