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Transcriptome profiling of Plasmodium vivax in Saimiri monkeys identifies potential ligands for invasion

Significance Plasmodium vivax infects humans by interacting with the Duffy blood group antigen (Duffy antigen) that is expressed on erythrocytes. Duffy antigen is absent in most Africans; hence, P. vivax infection is rare in Africa. However, low levels of P. vivax infections have been observed throughout Africa, suggesting that an alternative invasion pathway may be utilized to infect Africans. Duffy binding protein 1 binds to Aotus but not Saimiri erythrocytes, suggesting the involvement of an alternate invasion pathway in Saimiri infections. Hence, we performed comparative transcriptomics between Aotus- and Saimiri-infected P. vivax to identify these alternate invasion ligands. Transcriptomic analysis has identified genes belonging to tryptophan-rich antigen and merozoite surface protein families, which may play an important role in P. vivax infection in Africans. Unlike the case in Asia and Latin America, Plasmodium vivax infections are rare in sub-Saharan Africa due to the absence of the Duffy blood group antigen (Duffy antigen), the only known erythrocyte receptor for the P. vivax merozoite invasion ligand, Duffy binding protein 1 (DBP1). However, P. vivax infections have been documented in Duffy-negative individuals throughout Africa, suggesting that P. vivax may use ligands other than DBP1 to invade Duffy-negative erythrocytes through other receptors. To identify potential P. vivax ligands, we compared parasite gene expression in Saimiri and Aotus monkey erythrocytes infected with P. vivax Salvador I (Sal I). DBP1 binds Aotus but does not bind to Saimiri erythrocytes; thus, P. vivax Sal I must invade Saimiri erythrocytes independent of DBP1. Comparing RNA sequencing (RNAseq) data for late-stage infections in Saimiri and Aotus erythrocytes when invasion ligands are expressed, we identified genes that belong to tryptophan-rich antigen and merozoite surface protein 3 (MSP3) families that were more abundantly expressed in Saimiri infections compared with Aotus infections. These genes may encode potential ligands responsible for P. vivax infections of Duffy-negative Africans.