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The Koala Immune Response to Chlamydial Infection and Vaccine Development—Advancing Our Immunological Understanding

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The Koala Immune Response to Chlamydial Infection and Vaccine Development—Advancing Our Immunological Understanding animals Review The Koala Immune Response to Chlamydial Infection and Vaccine Development—Advancing Our Immunological Understanding Bonnie L Quigley 1 and Peter Timms 2,* 1 Provectus Algae, Noosaville, QLD 4566, Australia; [email protected] 2 Genecology Research Centre, University of the Sunshine Coast, Sippy Downs, QLD 4556, Australia * Correspondence: [email protected] Simple Summary: Chlamydia is a major pathogen of the Australian marsupial, the koala (Phascolarc- tos cinereus). One approach to improving this situation is to develop a vaccine. Human Chlamydia research suggests that an effective anti-chlamydial response will involve a balance between a cell- mediated Th1 response and a humoral Th2 responses, involving systemic IgG and mucosal IgA. Characterization of koalas with chlamydial disease suggests that increased expression for similar immunological pathways and monitoring of koalas’ post-vaccination can be successful and subse- quently lead to improved vaccines. These findings offer optimism that a chlamydial vaccine for wider distribution to koalas is not far off. Abstract: Chlamydia is a significant pathogen for many species, including the much-loved Australian marsupial, the koala (Phascolarctos cinereus). To combat this situation, focused research has gone into the development and refinement of a chlamydial vaccine for koalas. The foundation of this process has involved characterising the immune response of koalas to both natural chlamydial infection as well as vaccination. From parallels in human and mouse research, it is well-established that an effective Citation: Quigley, B.L.; Timms, P. anti-chlamydial response will involve a balance of cell-mediated Th1 responses involving interferon- The Koala Immune Response to Chlamydial Infection and Vaccine gamma (IFN-γ), humoral Th2 responses involving systemic IgG and mucosal IgA, and inflammatory Development—Advancing Our Th17 responses involving interleukin 17 (IL-17) and neutrophils. Characterisation of koalas with Immunological Understanding. chlamydial disease has shown increased expression within all three of these major immunological Animals 2021, 11, 380. https:// pathways and monitoring of koalas’ post-vaccination has detected further enhancements to these doi.org/10.3390/ani11020380 key pathways. These findings offer optimism that a chlamydial vaccine for wider distribution to koalas is not far off. Recent advances in marsupial genetic knowledge and general nucleic acid assay Academic Editor: Natalia Elguezabal technology have moved koala immunological research a step closer to other mammalian research Received: 11 December 2020 systems. However, koala-specific reagents to directly assay cytokine levels and cell-surface markers Accepted: 28 January 2021 are still needed to progress our understanding of koala immunology. Published: 3 February 2021 Keywords: koalas; vaccines; immunity; Chlamydia Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Chlamydia and Koalas Chlamydia are obligate intracellular bacteria recognised in a wide range of hosts. Traditionally identified and studied in birds, cattle, guinea pigs, sheep and humans [1], continued research has expanded the list of chlamydial hosts to include insects, amphibians, Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. molluscs, arachnids, reptiles, fish, and amoeba, as well as mammals like pigs, goats, deer, This article is an open access article cats, bats, possums, and koalas [2]. Chlamydial disease in the koala, Phascolarctos cinereus, distributed under the terms and has been particularly well studied, given the devastating toll it has taken on this iconic conditions of the Creative Commons Australian marsupial (Figure1)[ 3,4]. Chlamydial infection in koalas is dominated by the Attribution (CC BY) license (https:// species Chlamydia pecorum. These infections lead to ocular and urogenital/reproductive creativecommons.org/licenses/by/ diseases comparable to Chlamydia trachomatis infections in humans, which include kera- 4.0/). toconjunctivitis and scarring in the eye leading to blindness and cystitis/nephritis and Animals 2021, 11, 380. https://doi.org/10.3390/ani11020380 https://www.mdpi.com/journal/animals Animals 2021, 11, 380 2 of 10 Animals 2021, 11, x 2 of 11 reproductive cysts in the urogenital and reproductive tracts, respectively, leading to severe pain and infertility [3,4]. In both humans and koalas, vaccination has been identified as the most promising avenue of control for this pathogen [5]. However, despite years of research,research, nono commercialcommercial vaccine vaccine is is available available for for either either host. host. What What research research has has achieved achieved is ais greater a greater understanding understanding of theof the immune immune response response to chlamydial to chlamydial infection infection and and vaccination, vaccina- particularlytion, particularly in koalas, in koalas, setting setti theng stage the stage for future for future success. success. FigureFigure 1.1. KoalaKoala ((PhascolarctosPhascolarctos cinereuscinereus).). PhotoPhoto creditcredit BonnieBonnie Quigley.Quigley. MarsupialsMarsupials occupy a a unique unique branch branch of of the the mammalian mammalian evolutionary evolutionary tree, tree, having having di- divergedverged from from their their eutherian eutherian (placental) (placental) relatives relatives ~148 ~148 million million years years ago ago [6]. [ 6Originally]. Originally be- believedlieved to tohave have slower slower and and less less accentuated accentuated immune immune responses responses [7–9], [7 –it9 ],is itnow is now recognised recog- nisedthat the that immune the immune system system of marsupials of marsupials is just as is intricate just as intricate and complex and complex as that of as their that eu- of theirtherian eutherian counterparts counterparts [10]. While [10 ].study While into study the components into the components and general and development general devel- of opmentthe koala of immune the koala system immune has already system hasspanned already several spanned decades several of research decades (reviewed of research by (reviewed[11]), the complete by [11]), koala the complete genome koalahas only genome recently has been only sequenced recently been [12]. sequencedThis has meant [12]. Thisthat hasmuch meant of the that foundational much of the work foundational carried out work with carried koala outimmune with koalagenes immune and processes genes andwere processes based on were concepts based extrapolated on concepts from extrapolated more characterised from more characterisedmammalian systems. mammalian Ko- systems.ala-specific Koala-specific reagents for reagents experimentation for experimentation have also been have limited, also been given limited, the non-model given the non- or- modelganism organism status of statusthis marsupial. of this marsupial. However, However, despite despitethese limitations, these limitations, chlamydial chlamydial vaccine vaccinedevelopment development for koalas for has koalas progressed has progressed over the over last thedecade last decadeto generate to generate research research vaccine vaccineformulations formulations with very with promising very promising efficacies efficacies [13–15]. [13 Research–15]. Research has also has highlighted also highlighted many manysimilarities similarities in immune in immune responses responses to Chlamydia to Chlamydia infectioninfection between between hosts, hosts, allowing allowing forfor knowledgeknowledge fromfrom one one host host to to guide guide research research in in others. others. This This has has proven proven advantageous advantageous to the to koalathe koala in the in fieldthe field of chlamydial of chlamydial immune immune responses responses and and vaccine vaccine development. development. 2. Effective Chlamydial Immune Responses 2. Effective Chlamydial Immune Responses Chlamydial infection, disease, and vaccine research, often from human or mouse Chlamydial infection, disease, and vaccine research, often from human or mouse studies, has established a solid framework for what immune responses are necessary to clearstudies, and has prevent established chlamydial a solid infections. framework Additionally, for what immune chlamydial responses research are in necessary non-model to systems,clear and such prevent as non-human chlamydial primatesinfections. and Additionally, guinea pigs, chlamydial deserves recognition research in fornon-model also ad- vancingsystems, ocular such as chlamydial non-human disease primates understanding and guinea and pigs, vaccine deserves development recognition [16 for]. Overall,also ad- itvancing has become ocular well-established chlamydial disease that understanding a combined cellular and vaccine and humoral development immune [16]. response Overall, is neededit has become for complete well-established protection that from achlamydial combined cellular infection and and humoral disease immune progression response [17–19 is]. needed for complete protection from chlamydial infection and disease progression [17– 19]. Animals 2021, 11, 380 3 of 10 2.1. Immunogenetics For any adaptive immune response to be generated, an early key step is the presen- tation of chlamydial antigens to T cells via the major histocompatibility complex (MHC) or human leukocyte antigen (HLA) system. MHC molecules present antigens from either intracellular threats via class I molecules or
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