Abstract
Besnoitia besnoiti is an important obligate intracellular parasite of cattle which primarily infects host endothelial cells of blood vessels during the acute phase of infection. Similar to the closely related parasite Toxoplasma gondii, B. besnoiti has fast proliferating properties leading to rapid host cell lysis within 24–30 h p.i. in vitro. Some apicomplexan parasites were demonstrated to modulate the host cellular cell cycle to successfully perform their intracellular development. As such, we recently demonstrated that T. gondii tachyzoites induce G2/M arrest accompanied by chromosome missegregation, cell spindle alteration, formation of supernumerary centrosomes, and cytokinesis impairment when infecting primary bovine umbilical vein endothelial cells (BUVEC). Here, we follow a comparative approach by using the same host endothelial cell system for B. besnoiti infections. The current data showed that—in terms of host cell cycle modulation—infections of BUVEC by B. besnoiti tachyzoites indeed differ significantly from those by T. gondii. As such, cyclin expression patterns demonstrated a significant upregulation of cyclin E1 in B. besnoiti–infected BUVEC, thereby indicating parasite-driven host cell stasis at G1-to-S phase transition. In line, the mitotic phase of host cell cycle was not influenced since alterations of chromosome segregation, mitotic spindle formation, and cytokinesis were not observed. In contrast to respective T. gondii–related data, we furthermore found a significant upregulation of histone H3 (S10) phosphorylation in B. besnoiti–infected BUVEC, thereby indicating enhanced chromosome condensation to occur in these cells. In line to altered G1/S-transition, we here additionally showed that subcellular abundance of proliferating cell nuclear antigen (PCNA), a marker for G1 and S phase sub-stages, was affected by B. besnoiti since infected cells showed increased nuclear PCNA levels when compared with that of control cells.
Highlights
The apicomplexan obligate intracellular protozoa Besnoitia besnoiti represents a coccidian parasite of major importanceSection Editor: Panagiotis KaranisGiessen, Germany 5 German Center for Lung Research (DZL), Giessen, Germany in cattle industry
We recently reported that T. gondii infections of primary bovine umbilical vein endothelial cells (BUVEC) lead to a G2/M arrest and trigger severe defects during mitosis as propagated by chromosome missegregation, supernumerary centrosome formation, and cytokinesis impairment (Velásquez et al 2019)
This was tested via DRAQ5based live cell 3D holotomographic microscopy (3D Nanolive®). By this novel live cell imaging technique, we showed that B. besnoiti infections did not affect the nuclear phenotype, while T. gondii infections, which were used for comparative reasons, induced a binucleated phenotype in BUVEC (Fig. 1e)
Summary
The apicomplexan obligate intracellular protozoa Besnoitia besnoiti represents a coccidian parasite of major importanceSection Editor: Panagiotis KaranisGiessen, Germany 5 German Center for Lung Research (DZL), Giessen, Germany in cattle industry. Bovine besnoitiosis leads to severe skin alterations, vulvitis, vaginitis, orchitis, and infertility of bulls and cows among other signs (Gollnick et al 2018) This parasite causes significant losses in commercial cattle industry and impairs individual animal welfare (Dubey and Lindsay 1996; Dubey 2003; Cortes et al 2014). It is well-known that apicomplexan parasites significantly modulate their host cells to guarantee successful intracellular development and proliferation. As such, they influence numerous host cellular pathways, such as apoptosis, autophagy, cytoskeleton, metabolism, or immune reactions. The cell cycle of mammalian cells represents a highly regulated and complex processes that includes successive progression of distinct cell
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