A spatiotemporally resolved single-cell atlas of the Plasmodium liver stage

Amichay Afriat, Vanessa Zuzarte-Luís, Keren Bahar Halpern, Lisa Buchauer, Sofia Marques, Ângelo Ferreira Chora, Aparajita Lahree, Ido Amit, Maria M. Mota () and Shalev Itzkovitz ()
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Amichay Afriat: Weizmann Institute of Science
Vanessa Zuzarte-Luís: Faculdade de Medicina da Universidade de Lisboa
Keren Bahar Halpern: Weizmann Institute of Science
Lisa Buchauer: Weizmann Institute of Science
Sofia Marques: Faculdade de Medicina da Universidade de Lisboa
Ângelo Ferreira Chora: Faculdade de Medicina da Universidade de Lisboa
Aparajita Lahree: Faculdade de Medicina da Universidade de Lisboa
Ido Amit: Weizmann Institute of Science
Maria M. Mota: Faculdade de Medicina da Universidade de Lisboa
Shalev Itzkovitz: Weizmann Institute of Science

Nature, 2022, vol. 611, issue 7936, 563-569

Abstract: Abstract Malaria infection involves an obligatory, yet clinically silent liver stage1,2. Hepatocytes operate in repeating units termed lobules, exhibiting heterogeneous gene expression patterns along the lobule axis3, but the effects of hepatocyte zonation on parasite development at the molecular level remain unknown. Here we combine single-cell RNA sequencing4 and single-molecule transcript imaging5 to characterize the host and parasite temporal expression programmes in a zonally controlled manner for the rodent malaria parasite Plasmodium berghei ANKA. We identify differences in parasite gene expression in distinct zones, including potentially co-adaptive programmes related to iron and fatty acid metabolism. We find that parasites develop more rapidly in the pericentral lobule zones and identify a subpopulation of periportally biased hepatocytes that harbour abortive infections, reduced levels of Plasmodium transcripts and parasitophorous vacuole breakdown. These ‘abortive hepatocytes’, which appear predominantly with high parasite inoculum, upregulate immune recruitment and key signalling programmes. Our study provides a resource for understanding the liver stage of Plasmodium infection at high spatial resolution and highlights the heterogeneous behaviour of both the parasite and the host hepatocyte.

Date: 2022
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DOI: 10.1038/s41586-022-05406-5

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