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Cell Microbiol. 2019 Aug 30:e13112. doi: 10.1111/cmi.13112. [Epub ahead of print]

The apical annuli of Toxoplasma gondii are composed of coiled-coil and signalling proteins embedded in the inner membrane complex sutures.

Author information

1
Department of Biology, Boston College, Chestnut Hill, Massachusetts.
2
Precision Medicine Center, Department of Science, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi Province, China.
3
Department of Chemistry, Boston College, Chestnut Hill, Massachusetts.
4
Department of Biology, University of Puerto Rico, San Juan, Puerto Rico.

Abstract

The apical annuli are among the most intriguing and understudied structures in the cytoskeleton of the apicomplexan parasite Toxoplasma gondii. We mapped the proteome of the annuli in Toxoplasma by reciprocal proximity biotinylation (BioID), and validated five apical annuli proteins (AAP1-5), Centrin2, and an apical annuli methyltransferase. Moreover, inner membrane complex (IMC) suture proteins connecting the alveolar vesicles were also detected and support annuli residence within the sutures. Super-resolution microscopy identified a concentric organisation comprising four rings with diameters ranging from 200 to 400 nm. The high prevalence of domain signatures shared with centrosomal proteins in the AAPs together with Centrin2 suggests that the annuli are related and/or derived from the centrosomes. Phylogenetic analysis revealed that the AAPs are conserved narrowly in coccidian, apicomplexan parasites that multiply by an internal budding mechanism. This suggests a role in replication, for example, to provide pores in the mother IMC permitting exchange of building blocks and waste products. However, presence of multiple signalling domains and proteins are suggestive of additional functions. Knockout of AAP4, the most conserved compound forming the largest ring-like structure, modestly decreased parasite fitness in vitro but had no significant impact on acute virulence in vivo. In conclusion, the apical annuli are composed of coiled-coil and signalling proteins assembled in a pore-like structure crossing the IMC barrier maintained during internal budding.

KEYWORDS:

BioID; Toxoplasma gondii; apicomplexa; cytoskeleton; proteomics

PMID:
31470470
DOI:
10.1111/cmi.13112

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