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Harvard Thesis Template Functional Characterisation Of Novel Plasmodium falciparum Proteins And Their Role In Erythrocyte Invasion. Benjamin Liffner Research Centre for Infectious Diseases Department of Molecular and Biomedical Sciences School of Biological Sciences University of Adelaide August 2020 i A thesis submitted by Benjamin Liffner to The University of Adelaide, for fulfilment of the requirements for Doctor of Philosophy in Biological Sciences in the Department of Molecular and Biomedical Sciences, School of Biological Sciences. ii Abstract Malaria caused by Plasmodium falciparum is responsible for the deaths of hundreds of thousands of children every year, and imparts an overwhelming economic burden on the world’s poorest countries. All symptoms of malaria are caused during the asexual blood- stage of the P. falciparum lifecycle, which is reliant on merozoite invasion of host red blood cells (RBCs). Due to its essentiality for parasite survival, and its exposure to the host immune system, merozoite invasion is an attractive target for the development of antimalarial therapeutics. Merozoite invasion is coordinated by a series of secretory organelles, of which the largest and most well characterised are the rhoptries. Previous studies into rhoptry proteins have been strongly foccused on antigens that are secreted from the rhoptries during invasion; primarily due to their promise as vaccine candidates. As such, very little is known about proteins that coordinate rhoptry biogenesis, structure, or function. Prior to this study the P. falciparum proteins Pf3D7_0210600 and Pf3D7_0405200, hereafter referred to as P. falciparum Cytosolically Exposed Rhoptry Leaflet Interacting proteins (PfCERLI) 1 and 2, were largely uncharacterised proteins that previous studies had suggested may play a role in merozoite invasion. We hypothesised that PfCERLI1 and PfCERLI2 were rhoptry proteins that shared an evolutionary relationship and were both essential for merozoite invasion. We aimed to test these hypotheses through bioinformatic analyses, immunofluorescence microscopy, and gene disruption or inducible knockdown. Bioinformatic and phylogenetic analyses showed that cerli1 and cerli2 arose through an ancestral gene duplication of cerli1 that was present in the most recent common ancestor of haematozoa and coccidia. Analysis of the structure of CERLI proteins revealed iii they possess a conserved motif with the consensus sequence PHISE/DxxP that we have termed PHIS, along with conserved C2 and Pleckstrin homology (PH) domains that are likely ito have a role in membrane association. Using selection linked integration targeted gene disruption (SLI-TGD) we determined that both Pfcerli1 and Pfcerli2 were refractory to gene deletion and likely important for blood-stage growth. To assess their functions, we used an inducible protein knockdown system whereby the addition of glucosamine (GLCN) results in specific mRNA degradation prior to translation. Knockdown of either CERLI1 or CERLI2 resulted in growth inhibition caused by an inability of merozoites to invade RBCs. Immunofluorescnce microscopy and biochemical techniques revealed that both proteins are peripheral membrane proteins that localise to the cytosolic face of the rhoptry bulb. Rhoptry secretion assays showed that knockdown of PfCERLI1, but not PfCERLI2, leads to a defect in the secretion of key rhoptry antigens. By contrast, electron microscopy analysis of rhoptry size indicated a significant increase in rhoptry length following PfCERLI2 knockdown, but no change with PfCERLI1 knockdown. Semi-quantiative super-resolution microscopy analysis determined that knockdown of PfCERLI1 alters rhoptry antigen distribution, and it was shown that both PfCERLI1 and PfCERLI2 knockdown inhibit processing of key rhoptry antigens. The findings of these studies show that the previously uncharacterised proteins, PfCERLI1 and PfCERLI2, are related rhoptry proteins whose functions are essential for maintaining rhoptry morphology, rhoptry secretion, and rhoptry antigen processing. iv Declaration I certify that this work contains no material which has been accepted for the award of any other degree or diploma in my name, in any university or other tertiary institution and, to the best of my knowledge and belief, contains no material previously published or written by another person, except where due reference has been made in the text. In addition, I certify that no part of this work will, in the future, be used in a submission in my name, for any other degree or diploma in any university or other tertiary institution without the prior approval of the University of Adelaide and where applicable, any partner institution responsible for the joint-award of this degree. I acknowledge that copyright of published works contained within this thesis resides with the copyright holder(s) of those works. I also give permission for the digital version of my thesis to be made available on the web, via the University’s digital research repository, the Library Search and also through web search engines, unless permission has been granted by the University to restrict access for a period of time. I acknowledge the support I have received for my research through the provision of an Australian Government Research Training Program Scholarship. Signature: Date: 26th August 2020 v Publications Peer-reviewed publications to support this thesis: 1.Liffner B, Frölich S, Heinemann GK, Liu B, Dixon MWA, Gilberger T, Wilson DW. (2020). PfCERLI1 is a conserved rhoptry associated protein essential for Plasmodium falciparum merozoite invasion of erythrocytes. Nature Communications. Manuscripts in preparation to support this thesis: 1. Liffner B, Balbin JM, Heinemann GK, Strauss J, Liu B, Dixon MWA, Gilberger T, Wilson DW. Pfcerli2 arose through duplication of Pfcerli1 and is essential for merozoite invasion by the malaria parasite Plasmodium falciparum. Other publications from this candidature: 1. Burda PC, Corsskey T, Lauk K, Zuborg A, Söhnchen C, Liffner B, Wilcke L, Strauss J, Jeffries C, Svergun D, Wilson DW, Wilmanns M, Gilberger T. Structural analysis reveals a lipocalin in the malaria parasite Plasmodium falciparum that is essential for parasite proliferation. Cell Reports. 2. Wichers JS, Scholz J, Strauss J, Witt S, Lill A, Ehnold L, Neupert N, Liffner B, Lühken R, Petter M, Lorenzen S, Wilson DW, Löw C, Lavazec C, Bruchhaus I, Tannich E, Gilberger TW, Bachmann A. (2019). Dissecting the gene expression, localization, vi membrane topology and function of the Plasmodium falciparum STEVOR protein family. mBio. 3. Geiger M, Brown C, Wichers JS, Strauss J, Liffner B, Wilcke L, Lemcke S, Wilson DW, Filarsky M, Burda PC, Zhang K, Junoop M, Gilberger T. (2019). Structural insights into PfARO and characterization of its interaction with PfAIP. Journal of Molecular Biology. Other accepted manuscript from this candidature: 1. Burns A, Sleebs B, Ghizal S, De Paoli A, Anderson D, Liffner B, Harvey R, Beeson JG, Creek DJ, Goodman CD, McFadden GI, Wilson DW. Retargeting azithromycin-like compounds as antimalarials with dual modality. Accepted at BMC Biology (BMCB-D-20- 00228). vii Communications The results of this thesis were presented at the following scientific conferences: 1. Liffner B, Burns A, Wilson W. Characterising the role of PfROMP in erythrocyte invasion and sexual development of the malaria parasite, Plasmodium falciparum. Adelaide Protein Group Student Awards 2017, Adelaide, Australia. Poster Presentation. 2. Liffner B, Frölich S, Balbin JM, Lemcke S, Alder A, Gilberger T, Wilson DW. Understanding how the malaria parasite, Plasmodium falciparum, invades red blood cells. German Academic Exchange Service (DAAD) alumni meeting 2018, Melbourne, Australia. Poster presentation. 3. Liffner B, Heinemann GK, Gilbeger T, Wilson DW. Functional and structural insights into related essential rhoptry proteins. Biology and Pathology of the Malaria Parasite 2019, Heidelberg, Germany. Poster presentation and flash talk. 4. Liffner B, Frölich S, Beeson J, Gilberger T, Wilson DW. Genetic analysis of a conserved protein reveals an important role in Plasmodium falciparum merozoite invasion of the host cell. Biology and Pathology of the Malaria Parasite 2019, Heidelberg, Germany. Poster presentation and flash talk. 5. Liffner B, Frölich S, Liu B, Dixon MWA, Gilbeger T, Wilson DW. Functional analysis of a conserved rhoptry protein reveals an essential role in erythrocyte invasion by Plasmodium falciparum merozoites. Gordon Research Seminar: Malaria, 2019, Les Diablerets, Switzerland. Poster presentation. viii 6. Liffner B, Frölich S, Dixon MWA, Gilberger T, Wilson DW. Identification of a novel rhoptry protein that is essential for merozoite invasion. Malaria in Melbourne 2019, Melbourne, Australia. Oral presentation. 7. Liffner B, Frölich S, Balbin JM, Wilson DW. A novel malaria parasite protein essential for invasion. Institute for Photonics and Advanced Sensing Student Awards 2020, Adelaide, Australia. Oral presentation. 8. Liffner B, Frölich S, Dixon MWA, Heinemann G, Liu B, Ralph SA, Gilberger T, Wilson DW. Identification of a novel malaria merozoite protein that is essential for rhoptry secretion. Molecular Approaches to Malaria 2020, Lorne, Australia. Poster presentation. 9. Liffner B, Frölich S, Balbin JM, Strauss J, Dixon MWA, Heinemann G, Liu B, Ralph SA, Gilberger T, Wilson DW. Identification of related P. falciparum merozoite proteins that are essential for rhoptry secretion. Australian Society for Parasitology conference 2020. Oral Presentation. ix Acknowledgments
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