Comparative analysis of gene expression between Babesia bovis blood stages and kinetes allowed by improved genome annotation

Ueti, Massaro W.; Johnson, Wendell C.; Kappmeyer, Lowell S.; Herndon, David R.; Mousel, Michelle R.; Reif, Kathryn E.; Taus, Naomi S.; Ifeonu, Olukemi O.; Silva, Joana C.; Suárez, Carlos E.; Brayton, Kelly A.

doi:10.1016/j.ijpara.2020.08.006

Cited by 24 publications

(67 citation statements)

References 78 publications

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“…Upregulation of B. bovis cdpk4, ttl, and mt expression at day 6 after female tick dropping suggests that these genes may also be important in B. bovis kinete development. This agrees with a recent RNA-seq study that showed all three genes were highly upregulated in B. bovis kinetes [39]. It has been reported that XA is important for in vitro induction of Babesia sexual stages [8,10,40].…”

Section: Discussionsupporting

confidence: 93%

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Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Hussein

Johnson²,

Taus

et al. 2021

Parasites Vectors

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Background Babesia bovis is one of the most significant tick-transmitted pathogens of cattle worldwide. Babesia bovis parasites have a complex lifecycle, including development within the mammalian host and tick vector. Each life stage has developmental forms that differ in morphology and metabolism. Differentiation between these forms is highly regulated in response to changes in the parasite’s environment. Understanding the mechanisms by which Babesia parasites respond to environmental changes and the transmission cycle through the biological vector is critically important for developing bovine babesiosis control strategies. Results In this study, we induced B. bovis sexual stages in vitro using xanthurenic acid and documented changes in morphology and gene expression. In vitro induced B. bovis sexual stages displayed distinctive protrusive structures and surface ruffles. We also demonstrated the upregulation of B. bovis calcium-dependent protein kinase 4 (cdpk4), tubulin-tyrosine ligase (ttl), and methyltransferase (mt) genes by in vitro induced sexual stages and during parasite development within tick midguts. Conclusions Similar to other apicomplexan parasites, it is likely that B. bovis upregulated genes play a vital role in sexual reproduction and parasite transmission. Herein, we document the upregulation of cdpk4, ttl, and mt genes by both B. bovis in vitro induced sexual stages and parasites developing in the tick vector. Understanding the parasite's biology and identifying target genes essential for sexual reproduction will enable the production of non-transmissible live vaccines to control bovine babesiosis. Graphical abstract

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Section: Discussionsupporting

confidence: 93%

“…This agrees with a recent RNA-seq study that showed all three genes were highly upregulated in B . bovis kinetes [ 39 ].…”

Section: Discussionmentioning

confidence: 99%

Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Hussein

Johnson²,

Taus

et al. 2021

Parasites Vectors

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“…Here we have shown that BbVEAP knockdown merozoites have no defect in invasion ability and reduction of parasitemia is due to impaired development in the RBC. This gene is conserved across piroplasmida and is upregulated in B. bovis blood stage 27 In conclusion, the methodology of merozoite purification introduced in this paper is robust and could be a valuable tool to study B. bovis development in the RBC.…”

Section: Discussionmentioning

confidence: 87%

Isolation of viable Babesia bovis merozoites to study parasite invasion

Hakimi

Asada

Ishizaki

et al. 2021

Preprint

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Babesia parasite invades exclusively red blood cell (RBC) in mammalian host and induce alterations to host cell for survival. Despite the importance of Babesia in livestock industry and emerging cases in humans, their basic biology is hampered by lack of suitable biological tools. In this study, we aimed to develop a synchronization method for Babesia bovis which causes the most pathogenic form of bovine babesiosis. Initially, we used compound 2 (C2), a specific inhibitor of cyclic GMP-dependent protein kinase (PKG) and a derivative of C2, ML10. While both inhibitors were able to prevent B. bovis egress from RBC and increased percentage of binary forms, removal of inhibitors from culture did not result in a synchronized egress of parasites. Because using PKG inhibitors alone was not efficient to induce a synchronized culture, we isolated viable and invasive B. bovis merozoites and showed dynamics of merozoite invasion and development in RBCs. Using isolated merozoites we showed that BbVEAP, VESA1-export associated protein, is essential for parasite development in the RBC while has no role in invasion. Given the importance of invasion for establishment of infection, this study paves the way for finding novel antigens to be used in control strategies against bovine babesiosis.

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“…The analysis of gene regulation during B. bovis infection of mammalian host and tick vector was performed by using RNA-Seq data sets deposited in the NCBI Gene Expression Omnibus (GEO; ) under accession number GSE144066. Briefly, the datasets were generated from B. bovis blood stages isolated from infected calves and B. bovis kinete stages from female Ripicephalus microplus tick hemolymph as previously described [ 59 ]. Evaluation of up-regulation of the genes of interest was compared by the log 10 CPM of transcripts of the two B. bovis stages from vertebrate and invertebrate hosts.…”

Section: Methodsmentioning

confidence: 99%

N-Glycosylation in Piroplasmids: Diversity within Simplicity

et al. 2021

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N-glycosylation has remained mostly unexplored in Piroplasmida, an order of tick-transmitted pathogens of veterinary and medical relevance. Analysis of 11 piroplasmid genomes revealed three distinct scenarios regarding N-glycosylation: Babesia sensu stricto (s.s.) species add one or two N-acetylglucosamine (NAcGlc) molecules to proteins; Theileria equi and Cytauxzoon felis add (NAcGlc)2-mannose, while B. microti and Theileria s.s. synthesize dolichol-P-P-NAcGlc and dolichol-P-P-(NAcGlc)2 without subsequent transfer to proteins. All piroplasmids possess the gene complement needed for the synthesis of the N-glycosylation substrates, dolichol-P and sugar nucleotides. The oligosaccharyl transferase of Babesia species, T. equi and C. felis, is predicted to be composed of only two subunits, STT3 and Ost1. Occurrence of short N-glycans in B. bovis merozoites was experimentally demonstrated by fluorescence microscopy using a NAcGlc-specific lectin. In vitro growth of B. bovis was significantly impaired by tunicamycin, an inhibitor of N-glycosylation, indicating a relevant role for N-glycosylation in this pathogen. Finally, genes coding for N-glycosylation enzymes and substrate biosynthesis are transcribed in B. bovis blood and tick stages, suggesting that this pathway is biologically relevant throughout the parasite life cycle. Elucidation of the role/s exerted by N-glycans will increase our understanding of these successful parasites, for which improved control measures are needed.

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Comparative analysis of gene expression between Babesia bovis blood stages and kinetes allowed by improved genome annotation

Cited by 24 publications

References 78 publications

Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Differential expression of calcium-dependent protein kinase 4, tubulin tyrosine ligase, and methyltransferase by xanthurenic acid-induced Babesia bovis sexual stages

Isolation of viable Babesia bovis merozoites to study parasite invasion

N-Glycosylation in Piroplasmids: Diversity within Simplicity

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