Plasmodium falciparum sexual parasites develop in human erythroblasts and affect erythropoiesis.

Gaëlle Neveu; Cyrielle Richard; Florian Dupuy; Prativa Behera; Fiona Volpe; Pradeep Annamalai Subramani; Benjamin Marcel-Zerrougui; Patrice Vallin; Muriel Andrieu; Aruna Mukti Minz; +11 more... Nabih Azar; Rafael M Martins; Audrey Lorthiois; Florence Gazeau; José-Juan Lopez-Rubio; Dominique Mazier; Amanda KA Silva; Sanghamitra Satpathi; Samuel C Wassmer ORCID logo; Frédérique Verdier; Catherine Lavazec; (2020) Plasmodium falciparum sexual parasites develop in human erythroblasts and affect erythropoiesis. Blood, 136 (12). pp. 1381-1393. ISSN 0006-4971 DOI: 10.1182/blood.2019004746
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Plasmodium falciparum gametocytes, the sexual stage responsible for malaria parasite transmission from humans to mosquitoes, are key targets for malaria elimination. Immature gametocytes develop in the human bone marrow parenchyma, where they accumulate around erythroblastic islands. Notably though, the interactions between gametocytes and this hematopoietic niche have not been investigated. Here, we identify late erythroblasts as a new host cell for P falciparum sexual stages and show that gametocytes can fully develop inside these nucleated cells in vitro and in vivo, leading to infectious mature gametocytes within reticulocytes. Strikingly, we found that infection of erythroblasts by gametocytes and parasite-derived extracellular vesicles delay erythroid differentiation, thereby allowing gametocyte maturation to coincide with the release of their host cell from the bone marrow. Taken together, our findings highlight new mechanisms that are pivotal for the maintenance of immature gametocytes in the bone marrow and provide further insights on how Plasmodium parasites interfere with erythropoiesis and contribute to anemia in malaria patients.


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