Babesia bovis merozoites invade human, ovine, equine, porcine and caprine erythrocytes by a sialic acid-dependent mechanism followed by developmental arrest after a single round of cell fission.
Abstract: Babesia bovis infections have only been observed in bovine species in contrast to Babesia divergens that also can infect humans, sheep and rodents. Using an in vitro assay that assesses invasion of erythrocytes by free merozoites after a 1-h incubation period, it was shown that specificity is not determined by host-specific interactions associated with invasion. Human erythrocytes were invaded more efficiently than bovine erythrocytes whereas erythrocytes of sheep, pigs and horses were invaded only slightly less efficiently. In contrast, goat erythrocytes were refractory to efficient invasion. Significant differences in invasion efficiency into erythrocytes from different individuals of the same species were observed. Erythrocytes from all species, except for goats, supported intracellular development of newly invaded merozoites and high numbers of duplicated parasites, located in a morphologically normal accole position, were present. Only in bovine erythrocytes did subsequent rounds of invasion, leading to increased parasitaemia, take place. This suggests that host specificity is determined by factors operating late in the erythrocytic stage of the B. bovis life cycle. Incubation of erythrocytes with neuraminidase prior to invasion led to a decrease in invasion efficiency of approximately 80%. This effect was observed for several species. The removal of either alpha(2-3)-linked or alpha(2-6)-linked sialic acid residues gave similar levels of reduction whereas simultaneous removal did not show an additive effect. Pre-incubation of merozoites with N-acetylneuraminyl-lactose decreased invasion efficiency by approximately 45% whereas addition just prior to invasion had no significant effect. The results demonstrate that invasion is dependent on the presence of sialic-acid containing membrane receptors on erythrocytes that interact with merozoite ligands that are probably already accessible during pre-incubation prior to invasion.
Publication Date: 2003-11-26 PubMed ID: 14636675DOI: 10.1016/s0020-7519(03)00254-6Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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This research investigates the specificity of Babesia bovis parasites in invading erythrocytes (red blood cells) of humans and various animals, and the role of sialic acid in this process. The study finds that all but goat erythrocytes support parasite growth and development, yet repeated invasion only takes place in bovine cells, suggesting host specificity happens late in the parasite’s lifecycle.
Study Rationale and Method
- While Babesia bovis infections are typically limited to bovines, unlike the more indiscriminate Babesia divergens, the aim of this research was to establish whether this discrimination happens during the initial invasion of host cells.
- An in vitro assay was used to measure erythrocyte invasion by free merozoites, which are a stage in the parasite’s lifecycle, within an hour.
Findings on Erythrocyte Invasion
- Human erythrocytes were found to be the most susceptible to invasion, ahead of bovine erythrocytes. Erythrocytes from sheep, pigs, and horses were slightly less affected, while goat erythrocytes were largely refractory to invasion.
- The level of invasion varied substantially amongst individuals from the same species.
- All species apart from goats supported intracellular development of the parasites, seen as a high number of duplicated parasites.
- Only in bovine erythrocytes did the parasites continue to invade in further rounds, leading to a larger parasite population, suggesting that host specificity emerges later in the parasite’s lifecycle.
The Role of Sialic Acid
- Erythrocyte treatment with neuraminidase, an enzyme that removes sialic acid from cells, resulted in an 80% reduction in invasion efficiency across most species. Removing either type of sialic acid molecule yielded similar results, and simultaneous removal did not compound the effect.
- Pre-treatment of merozoites with N-acetylneuraminyl-lactose, a sialic acid compound, resulted in a 45% reduction in invasion efficiency. Applying it just before invasion does not significantly alter the result.
- This evidence suggests that the invasion of erythrocytes by Babesia bovis merozoites is largely dependent on sialic acid-containing receptors on the erythrocyte membrane that interact with merozoite ligands—proteins that bind with specific cellular agents.
Cite This Article
APA
Gaffar FR, Franssen FF, de Vries E.
(2003).
Babesia bovis merozoites invade human, ovine, equine, porcine and caprine erythrocytes by a sialic acid-dependent mechanism followed by developmental arrest after a single round of cell fission.
Int J Parasitol, 33(14), 1595-1603.
https://doi.org/10.1016/s0020-7519(03)00254-6 Publication
Researcher Affiliations
- Division of Parasitology and Tropical Veterinary Medicine, Department of Infectious Diseases and Immunology, Utrecht University, P.O. Box 80165, 3508 TD Utrecht, The Netherlands.
MeSH Terms
- Animals
- Babesia bovis / physiology
- Babesiosis / parasitology
- Cattle
- Cattle Diseases / parasitology
- Erythrocyte Membrane / parasitology
- Goat Diseases / parasitology
- Goats
- Horse Diseases / parasitology
- Horses
- Host-Parasite Interactions
- Humans
- N-Acetylneuraminic Acid / metabolism
- Receptors, Cell Surface / metabolism
- Sheep
- Sheep Diseases / parasitology
- Species Specificity
- Swine
- Swine Diseases / parasitology
Citations
This article has been cited 6 times.- Cuy-Chaparro L, Bohórquez MD, Arévalo-Pinzón G, Castañeda-Ramírez JJ, Suárez CF, Pabón L, Ordóñez D, Gallego-López GM, Suárez CE, Moreno-Pérez DA, Patarroyo MA. Babesia Bovis Ligand-Receptor Interaction: AMA-1 Contains Small Regions Governing Bovine Erythrocyte Binding.. Int J Mol Sci 2021 Jan 13;22(2).
- Jouglin M, Fernández-de-Mera IG, de la Cotte N, Ruiz-Fons F, Gortázar C, Moreau E, Bastian S, de la Fuente J, Malandrin L. Isolation and characterization of Babesia pecorum sp. nov. from farmed red deer (Cervus elaphus).. Vet Res 2014 Aug 26;45(1):78.
- Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Abtahi Froushani SM, Arjmand J, Golabi M. Serum concentration of sialic acids in naturally occurring ovine babesiosis.. Trop Anim Health Prod 2014 Oct;46(7):1217-21.
- Chauvin A, Moreau E, Bonnet S, Plantard O, Malandrin L. Babesia and its hosts: adaptation to long-lasting interactions as a way to achieve efficient transmission.. Vet Res 2009 Mar-Apr;40(2):37.
- Malandrin L, Jouglin M, Moreau E, Chauvin A. Individual heterogeneity in erythrocyte susceptibility to Babesia divergens is a critical factor for the outcome of experimental spleen-intact sheep infections.. Vet Res 2009 Jul-Aug;40(4):25.
- Lobo CA. Babesia divergens and Plasmodium falciparum use common receptors, glycophorins A and B, to invade the human red blood cell.. Infect Immun 2005 Jan;73(1):649-51.
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