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Cell cycle-dependent phosphorylation of Theileria annulata schizont surface proteins

Wiens, O; Xia, D; Von Schubert, C; Wastling, J M; Dobbelaere, D A; Heussler, V T; Woods, K L

Authors

O Wiens

D Xia

C Von Schubert

J M Wastling

D A Dobbelaere

V T Heussler

K L Woods



Abstract

The invasion of Theileria sporozoites into bovine leukocytes is rapidly followed by the destruction of the surrounding host cell membrane, allowing the parasite to establish its niche within the host cell cytoplasm. Theileria infection induces host cell transformation, characterised by increased host cell proliferation and invasiveness, and the activation of anti-apoptotic genes. This process is strictly dependent on the presence of a viable parasite. Several host cell kinases, including PI3-K, JNK, CK2 and Src-family kinases, are constitutively activated in Theileria-infected cells and contribute to the transformed phenotype. Although a number of host cell molecules, including IkB kinase and polo-like kinase 1 (Plk1), are recruited to the schizont surface, very little is known about the schizont molecules involved in host-parasite interactions. In this study we used immunofluorescence to detect phosphorylated threonine (p-Thr), serine (p-Ser) and threonine-proline (p-Thr-Pro) epitopes on the schizont during host cell cycle progression, revealing extensive schizont phosphorylation during host cell interphase. Furthermore, we established a quick protocol to isolate schizonts from infected macrophages following synchronisation in S-phase or mitosis, and used mass spectrometry to detect phosphorylated schizont proteins. In total, 65 phosphorylated Theileria proteins were detected, 15 of which are potentially secreted or expressed on the surface of the schizont and thus may be targets for host cell kinases. In particular, we describe the cell cycle-dependent phosphorylation of two T. annulata surface proteins, TaSP and p104, both of which are highly phosphorylated during host cell S-phase. TaSP and p104 are involved in mediating interactions between the parasite and the host cell cytoskeleton, which is crucial for the persistence of the parasite within the dividing host cell and the maintenance of the transformed state.

Citation

Wiens, O., Xia, D., Von Schubert, C., Wastling, J. M., Dobbelaere, D. A., Heussler, V. T., & Woods, K. L. (2017). Cell cycle-dependent phosphorylation of Theileria annulata schizont surface proteins. PLoS ONE, 9(7), e103821. https://doi.org/10.1371/journal.pone.0103821

Journal Article Type Article
Acceptance Date Jul 7, 2014
Publication Date Jul 31, 2017
Deposit Date Jul 21, 2018
Publicly Available Date Mar 29, 2024
Journal PLoS One
Publisher Public Library of Science
Peer Reviewed Peer Reviewed
Volume 9
Issue 7
Pages e103821
DOI https://doi.org/10.1371/journal.pone.0103821
Public URL https://rvc-repository.worktribe.com/output/1391063

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