ALBA4 modulates its stage‐specific interactions and specific mRNA fates during Plasmodium yoelii growth and transmission

• Published in: Molecular microbiology 2017-10, Vol.106 (2), p.266-284
• Main Authors: Muñoz, Elyse E., Hart, Kevin J., Walker, Michael P., Kennedy, Mark F., Shipley, Mackenzie M., Lindner, Scott E.
• Format: Article
• Language: English
• Subjects: Animals; Anopheles - parasitology; Aquatic insects; Blood; Contamination; Disease transmission; Enzyme Repression; Malaria; Malaria - parasitology; Parasites; Parasitic Diseases - genetics; Plasmodium; Plasmodium yoelii - genetics; Plasmodium yoelii - growth & development; Plasmodium yoelii - physiology; Proteomics; Protozoan Proteins - metabolism; Ribonucleic acid; RNA; RNA, Messenger - biosynthesis; RNA, Messenger - metabolism; RNA-binding protein; RNA-Binding Proteins - metabolism; Sporozoites - metabolism; Transcriptome; Vector-borne diseases
• ISSN: 0950-382X; 1365-2958
• DOI: 10.1111/mmi.13762

Summary Transmission of the malaria parasite occurs in an unpredictable moment, when a mosquito takes a blood meal. Plasmodium has therefore evolved strategies to prepare for transmission, including translationally repressing and protecting mRNAs needed to establish the infection. However, mechanisms underlying these critical controls are not well understood, including whether Plasmodium changes its translationally repressive complexes and mRNA targets in different stages. Efforts to understand this have been stymied by severe technical limitations due to substantial mosquito contamination of samples. Here using P. yoelii, for the first time we provide a proteomic comparison of a protein complex across asexual blood, sexual and sporozoite stages, along with a transcriptomic comparison of the mRNAs that are affected in these stages. We find that the Apicomplexan‐specific ALBA4 RNA‐binding protein acts to regulate development of the parasite's transmission stages, and that ALBA4 associates with both stage‐specific and stage‐independent partners to produce opposing mRNA fates. These efforts expand our understanding and ability to interrogate both sexual and sporozoite transmission stages and the molecular preparations they evolved to perpetuate their infectious cycle. The apicomplexan‐specific RNA‐binding protein ALBA4 is important to both transmission stages in Plasmodium yoelii parasites. Comparative RNA‐seq and IP/mass spectrometry reveals that it may accomplish this through stage‐specific and stage‐independent protein interactions, ultimately producing opposing effects upon mRNAs in different stages. This work is the first to compare the proteomics and related transcriptomics of a protein complex across asexual blood, sexual blood and sporozoite stages in a malaria parasite.