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Robert Barigye A STUDY OF VIRAL TISSUE TROPISM AND CYTOKINE EXPRESSION IN BOVINE EPHEMERAL FEVER ROBERT BARIGYE BVetMed, MSc, PhD, MANZCVS (Path) A thesis submitted for the degree of Master of Philosophy at The University of Queensland in February 2020 School of Veterinary Science ABSTRACT While the clinical and pathological aspects of Bovine Ephemeral Fever (BEF) have been studied in cattle, major gaps still remain in our understanding of the pathogenesis of the disease. In particular, the cytokine networks that underlie fever and inflammation during acute BEF, and mechanisms that mediate the nascent adaptive immune response have not been empirically defined. In addition, the potential in vivo replication sites of BEFV, and the mechanistic events that underlie the paresis and chronic paralysis in some field BEF cases have also not been defined. The objectives of this research were: (1) to characterise the plasma kinetics of proinflammatory cytokines (IL-1β, IL-6, TNF-α) and IL-10 during natural BEFV infections in cattle; (2) to evaluate the plasma kinetics of IL-2, IFN-γ, IL-6, and IL-10 during the period of innate-immune response transition; and (3) to determine the overall tissue tropism and potential replication sites, along with assessing the likelihood of neurotropism of BEFV in naturally infected cattle. For the cytokine expression studies, experiments were carried out on two different cohorts of animals raised at two farms at different time points. Briefly, plasma from three BEFV-infected and three uninfected cattle was tested by cytokine-specific cELISA, viraemia monitored by qRT-PCR, and virus neutralising antibody titres determined using a standard protocol. Similarly, plasma from another four virus-infected and uninfected negative control animals was tested for the four study cytokines (IL-2, IFN-γ, IL-6, and IL-10), and viraemia and virus neutralising antibody titres determined. Biological specimens from nine adult cattle that died or were euthanised at different time points following natural BEFV infections were tested for viral antigen and RNA by IHC and qRT-PCR, respectively. In addition, virus isolation in autogenously derived splenic and haemal node cultures, and electron microscopic examination of ultrathin i sections from various tissues taken from the steer necropsied seven days after BEF diagnosis were performed. For the neurotropism studies, fresh brain, spinal cord, peripheral nerve, and other tissues were collected from four paralysed and six asymptomatic but virus-infected cattle and tested for viral RNA by qRT-PCR. Formalin-fixed tissues were routinely evaluated for histomorphological lesions and for viral antigen presence and distribution by IHC. Unlike the negative controls, plasma concentrations of IL-1β, TNF-α, IL-6, and IL-10 were consistently increased in the three virus-infected animals. Two of these heifers were recumbent and pyrexic on the first day of monitoring and increased cytokine production was already in progress by the time viraemia was detected in all the three infected animals. In all the virus-infected heifers, IL-1β was the most strongly expressed cytokine, IL-6 and IL-10 manifested intermediate plasma concentrations while TNF-α was the least expressed and demonstrated bi-phasic peaks three and five days after the onset of pyrexia. In two of the BEFV-infected heifers, viraemia resolved on the day of seroconversion while in the other infected animal, it resolved up to three days after seroconversion. In the second cohort of study cattle, unlike the negative controls, plasma IL-6 and IL-10 were increased in all the virus-infected animals starting several days prior to initiation of viraemia. In one animal, plasma IL-2 and IFN-γ levels were consistently higher than in the other three virus-infected animals. Notably, this animal had the shortest viraemia while the heifer with the lowest IL- 2/IFN-γ levels demonstrated the longest viraemia. For the virus-tissue tropism studies, BEFV antigens were detected in several tissues/organs in all the study cattle and both virus antigen and RNA were simultaneously demonstrated in the spleen and/or haemal node from 7/9 cattle; the longest period of RNA detection was in the haemal node 120 days following the initial BEF diagnosis. Overall, viral proteins ii were distributed intracytoplasmically within cells morphologically consistent with macrophages, neutrophils, dendritic cell-like cells and spindle shaped cells with a perivascular location. While definitive identification of the antigen-laden cells would have been informative, attempts at immunophenotyping were fruitless presumably due to antigen denaturation as the tests were done long after completion of the major experiments. In the case study steer necropsied within seven days from the day of definitive BEF diagnosis, viral RNA was detected in fresh spleen, haemal node, prefemoral lymph node, synovial fluid and in 13 spleen-derived cell cultures. In this animal, BEFV was isolated from autogenously derived splenic primary cell cultures six days after cessation of viraemia, and characteristic bullet-shaped virions confirmed in the haemal node by TEM. The neurotropism of BEFV was confirmed in the brain and peripheral nerves by IHC, while peripheral neuropathy was histologically demonstrated in three paralysed but not the six virus-infected animals not showing neurological signs. Wallerian degeneration (WD) was present in the lumbar spinal cord of a paralysed steer and in the cervical and thoracic spinal cord segments of three paralysed animals. While no spinal cord lesions were seen in the steer euthanised within seven days of illness, peripheral neuropathy was present and more severe in nerves of the brachial plexuses than in the gluteal or fibular nerves. The only steer with WD in the lumbar spinal cord also showed intrahistiocytic cell viral antigen that was spatially distributed within areas of moderate brain stem encephalitis. The present data documented variable increase in plasma IL-1β, IL-6, TNF-α, and IL-10 during natural BEFV infections with apparent upregulation of all but TNF-α appearing to precede seroconversion. Considering the anti-inflammatory properties of IL-10, its upregulation suggests a probable modulatory role that may potentially antagonise the fever response in animals acutely infected with BEFV. As iii the increase in plasma IL-6 and IL-10 appeared to precede seroconversion, the two cytokines may influence immunological events that pave way to B-cell activation and seroconversion. While remarkable variability in IL-2 and IFN-γ expression was seen in virus-infected animals, the increase in plasma levels of the two cytokines was associated with a shorter viraemia suggesting that, in addition to virus neutralising antibodies, IL-2 and IFN-γ-mediated cellular mechanisms may be required for resolution of viraemia in BEF. Based on these data, BEFV appears to have preferential tropism for bovine lymphoid tissues, and the spleen and haemal node may particularly be potential in vivo sites for BEFV replication. The present data also confirm that BEFV is neurotropic in cattle and that, in addition to WD in the spinal cord, peripheral neuropathy and non-suppurative brain stem encephalitis may contribute to chronic paralysis seen in BEFV-infected downer cattle. Additional studies are needed to define the precise role of T cells in anti-BEFV adaptive immune responses. The potential in vivo replication sites of the BEFV in cattle could be further characterised by in situ hybridisation and other molecular tools. iv DECLARATION BY AUTHOR This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others towards the jointly- authored works that I have included in this thesis. I have also clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis does not include any work that has previously been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis may be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate, I have obtained copyright permission from the copyright holder to reproduce material in this thesis. v PUBLICATIONS THAT ARE INCLUDED IN THE THESIS Per UQ Authorship Policy (PPL 4.20.04 Authorship), contributions of all co-authors to the above publications are briefly described in the table below. I) Publication citations – incorporated as Chapter 2. BARIGYE, R., MELVILLE, L.F., DAVIS, S., WALSH. S., HUNT, N., HUNT, R., ELLIOTT, N. 2015. Kinetics of pro-inflammatory cytokines, interleukin-10, and virus neutralising antibodies during acute ephemeral fever virus infections in Brahman cattle. Veterinary Immunology and Immunopathology 168:159-163. BARIGYE, R., MELVILLE, L.F., DAVIS, S., WALSH, S., HUNT, N., HUNT, R. 2016. Kinetics
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