Cycle of bovine lymphoblastoid cells parasitised by Theileria parva

Irvin, A.D.; Ocama, J.G.R.; Spooner, P.R.

doi:10.1016/s0034-5288(18)32305-1

Cited by 45 publications

(17 citation statements)

References 15 publications

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“…In general histone synthesis coincides with DNA synthesis, and an increase in histone expression has been described during S phase in mammalian cells [44]. It was previously shown that T. parva initiates DNA synthesis when the host cell is in mitosis [45], although this has never been tested for T. annulata . We therefore analysed the incorporation of the thymidine analogue 5-bromo-2-deoxyuridine (BrdU) into host and parasite nuclei while cells were released from S-phase-block.…”

Section: Resultsmentioning

confidence: 99%

Cell Cycle-Dependent Phosphorylation of Theileria annulata Schizont Surface Proteins

et al. 2014

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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.

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Section: Resultsmentioning

confidence: 99%

Cell Cycle-Dependent Phosphorylation of Theileria annulata Schizont Surface Proteins

et al. 2014

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“…Although the S phases of parasite and host are not synchronized, reports regarding synchronicity of parasite and host cell nuclear division are contradictory, with Irvin et al 1982 claiming a synchronization of the parasite nuclear division with host cell metaphase, while Hulliger et al 1964 found no proof for synchronization of the parasite division with any stage of the host cell cycle. With respect to the distribution of the schizont into daughter cells, it has been postulated that this is a random event (Hulliger et al 1964), although, considering that in normal cultures up to 95% of the cells usually harbour the parasite (Dobbelaere and Heussler 1999), a controlled process would appear to be more probable and more suitable for the parasite's purpose.…”

Section: Introductionmentioning

confidence: 99%

“…Within the leucocyte, the schizont displays deoxyribonucleic acid (DNA) synthesis asynchronous to the host cell (Irvin et al 1982). Although the S phases of parasite and host are not synchronized, reports regarding synchronicity of parasite and host cell nuclear division are contradictory, with Irvin et al 1982 claiming a synchronization of the parasite nuclear division with host cell metaphase, while Hulliger et al 1964 found no proof for synchronization of the parasite division with any stage of the host cell cycle.…”

Section: Introductionmentioning

confidence: 99%

Identification, molecular characterization and subcellular localization of a Theileria annulata parasite protein secreted into the host cell cytoplasm

et al. 2007

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Intracellular leucoproliferative Theileria are unique as eukaryotic organisms that transform the immune cells of their ruminant host. Theileria utilize the uncontrolled proliferation for rapid multiplication and distribution into host daughter cells. The equal distribution of the schizont into the daughter cells is thought to be accomplished by a tight association with the host cell mitotic apparatus. In this study, we describe a highly conserved novel 37 kD Theileria annulata protein (TaSE). TaSE was found to be localized inside the parasite, the parasite membrane and within the host cell cytoplasm. Moreover, it co-localized at distinct points with host cell microtubules, which was especially apparent during mitosis, where co-localization was found with the centromere, the mitotic spindle and the midbody. Association of TaSE with the host cell tubulin network was corroborated by coimmunoprecipitation and transient transfection experiments. This is the first description of a theilerial protein co-localizing and potentially interacting with a host cell protein. The distribution of TaSE during mitosis makes it a protein to consider as playing a potential role for parasite distribution into daughter host cells.

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“…Within the transformed cells the parasites undergo nuclear division ahead of the host cell due to a shortened or absent G2 phase. This enables the parasites to grow synchronously with their host cells and ensures the transfer of the parasites into daughter cells (Irvin et al 1982). This transformation, however, is completely reversible, since the infected cells return to a resting phenotype after the elimination of the parasite by the anti-theilerial drug buparvaquone (McHardy 1984;Rintelen et al 1990).…”

Section: Discussionmentioning

confidence: 99%

The proliferation-associated nuclear protein Ki-67 in the bovine system: partial characterisation and its application for determination of the proliferation of Theileria -infected bovine cells

Shayan

Gerlach

Hügel

et al. 1999

Parasitology Research

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Theileria annulata-infected bovine cells as well as mitogen-stimulated bovine peripheral blood mononuclear cells (PBMC) express a proliferation-associated nuclear protein equivalent to the human Ki-67 protein. In analogy to the human system, the expression of the bovine Ki-67 protein is restricted to proliferating cells only, since (a) Ki-67 expression paralleled [3H]-thymidine incorporation in concanavalin A (Con A)-stimulated bovine PBMC, (b) Ki-67 was not detectable in quiescent bovine cells, and (c) Ki-67 expression in Theileria-infected cells is related to the presence of the parasites within the cytoplasm of the host cells; upon treatment with the theilericidal drug buparvaquone the parasites are destroyed and the cells cease to proliferate and to express the Ki-67 protein. Western-blot analysis of lysates of proliferating bovine cells revealed that the prototype monoclonal antibody Ki-67 and the new equivalent antibody MIB-1 detected one prominent protein band with an apparent molecular weight of 430 kDa. Two cDNA clones (pUC18.B1.Ki-67 and pUC18.B2.Ki-67) were isolated from a lambdagt11 cDNA library of T. annulata-infected bovine cells by immunoscreening with the monoclonal antibody MIB-1. Comparison of these cDNA sequences with those of the human Ki-67 protein revealed 60-70% identity. Within the "Ki-67 motif", identity proved to be 80% at the amino acid level. The remarkable identity between bovine and human Ki-67 proteins suggests that MIB-1 can be used as a marker for cell proliferation in animal research. In this context we could identify proliferating cells in lymph nodes of Theileria-infected animals and, furthermore, we could distinguish between infected and uninfected proliferating cells using MIB-1 and an antiserum against a recombinant parasite protein designated SA288.

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Cycle of bovine lymphoblastoid cells parasitised by Theileria parva

Cited by 45 publications

References 15 publications

Cell Cycle-Dependent Phosphorylation of Theileria annulata Schizont Surface Proteins

Cell Cycle-Dependent Phosphorylation of Theileria annulata Schizont Surface Proteins

Identification, molecular characterization and subcellular localization of a Theileria annulata parasite protein secreted into the host cell cytoplasm

The proliferation-associated nuclear protein Ki-67 in the bovine system: partial characterisation and its application for determination of the proliferation of Theileria -infected bovine cells

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