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African Trypanosomes Mathieu Cayla†, Federico Rojas†, Eleanor Silvester†, Frank Venter† and Keith R

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African Trypanosomes Mathieu Cayla†, Federico Rojas†, Eleanor Silvester†, Frank Venter† and Keith R Cayla et al. Parasites Vectors (2019) 12:190 https://doi.org/10.1186/s13071-019-3355-5 Parasites & Vectors PRIMER Open Access African trypanosomes Mathieu Cayla†, Federico Rojas†, Eleanor Silvester†, Frank Venter† and Keith R. Matthews*† Abstract African trypanosomes cause human African trypanosomiasis and animal African trypanosomiasis. They are transmit- ted by tsetse fies in sub-Saharan Africa. Although most famous for their mechanisms of immune evasion by antigenic variation, there have been recent important studies that illuminate important aspects of the biology of these para- sites both in their mammalian host and during passage through their tsetse fy vector. This Primer overviews current research themes focused on these parasites and discusses how these biological insights and the development of new technologies to interrogate gene function are being used in the search for new approaches to control the parasite. The new insights into the biology of trypanosomes in their host and vector highlight that we are in a ‘golden age’ of discovery for these fascinating parasites. Keywords: Trypanosoma brucei, Sleeping sickness, Trypanosome What are trypanosomes? morphotypes exist, slender and stumpy forms [10, 11]. Te Trypanosomatidae (Phylum Euglenozoa) are obligate Slender forms evade the mammalian antibody response parasitic protozoans, which infect all vertebrate classes, through antigenic variation, entailing expression of a in addition to insects and plants. Trypanosomatids are variable surface glycoprotein (VSG) monolayer which unifagellated, and like other organisms in the order Kine- covers the trypanosome cell. Changes in the expression toplastida, are characterised by a modifed mitochondrial of VSG genes generate antigenically distinct subpopula- genome known as the kinetoplast [1, 2]. Tis is composed tions, which can evade the host immune response, and of DNA ‘mini’- and ‘maxicircles’ [3, 4], which can vary in so sustain the parasite infection [12, 13]. Te transition number and catenation depending on the particular spe- from slender to stumpy forms is regulated by a quorum cies [5]. Among the trypanosomatids, Trypanosoma is a sensing (QS) type process which prolongs host survival genus of particular medical and veterinary concern [6, 7]. and promotes transmission because stumpy forms are Te Salivaria group of trypanosomes, so named for being non-proliferative in the blood, but preferentially survive transmitted in the infected saliva of a tsetse fy vector in and colonise the tsetse midgut. (Glossina spp.), is represented by Trypanosoma brucei, While T. brucei is certainly a model for trypanosome T. congolense and T. vivax. Te former is the most well- biology, and indeed that of other kinetoplastids, sig- studied of the salivarian trypanosomes, with subspecies nifcant variation in morphology, transmission, and life- T. b. gambiense and T. b. rhodesiense being the causa- cycle, exists between diferent trypanosome species. tive agents of human African trypanosomiases (HAT). Neither T. vivax nor T. congolense, for example, (both Te dixenous life-cycle of T. brucei comprises vertebrate causing animal African trypanosomiasis, AAT), show stages and tsetse stages, which involves diferentiation morphological diferentiation in the bloodstream, though through a number of morphological forms, accompanied both exhibit density-dependent growth control [14, 15]. by remodelling of gene expression and metabolic pro- Also, T. b. equiperdum has circumvented the need for an cesses [8, 9] (Additional fle 1). In the bloodstream, two arthropod vector altogether, and instead is sexually trans- mitted between equines. Exciting advances in our under- standing of trypanosome biology continue to be made, *Correspondence: [email protected] †Mathieu Cayla, Federico Rojas, Eleanor Silvester, Frank Venter and Keith R. in addition to the development of new tools for studying Matthews contributed equally to this work these organisms. Tis Primer will highlight important Institute for Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, UK © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cayla et al. Parasites Vectors (2019) 12:190 Page 2 of 8 recent advances in this feld, as well as identifying areas being enriched in histone modifcations H4K10ac and that warrant investigation in future. H3K4me3 and four diferent histone variants that are also found at convergent transcription strand switch Why study the biology of trypanosomes? regions [32]. Trypanosomatids diverged from other eukaryotic line- Trypanosoma brucei also possesses a uniquely ages at least 500 million years ago and so provide a valua- evolved multifunctional RNAP I system, responsible for ble model for evolutionarily distinct eukaryotic processes the transcription of ribosomal gene units, as well as the [16, 17]. Despite their divergence, they exhibit tractable major surface proteins procyclins (expressed on tsetse and fascinating biology in terms of their nuclear and midgut forms) and bloodstream VSG genes [33, 34]. nucleosome architecture/substructures, transcription, It is estimated that there are around 10 million copies organellar segregation, DNA replication, developmen- of VSGs on the surface of a parasite shielding invari- tal biology and fagellar motility, for example [18, 19]. ant surface proteins [35–37]. Trypanosoma brucei pos- Tis tractability has been greatly assisted by the capac- sesses ~2500 VSG genes or pseudogenes [24], located in ity to culture trypanosomatids, to generate diferent life- subtelomeric regions of the chromosomes (comprising cycle stages and by the development of advanced genetic ~30% of the genome) [12, 38]. It is now understood that tools. Inducible systems for the regulated ectopic expres- during the course of an infection there are up to 100 sion of genes, or RNAi mediated knockdown have been VSGs that are expressed in the population at a peak of widely exploited, with CRISPR-Cas9 genome editing infection with a few variants dominating at each peak, [20, 21] recently added to the already large toolbox avail- allowing immune evasion [13, 39]. In the bloodstream able to manipulate trypanosomatid genomes and gene stage, there are ~15 telomeric VSG expression sites expression. As well as their intrinsically interesting biol- (ES), each containing 8–9 ES associated genes (ESAGs), ogy, trypanosomes remain important causes of disease. 70 bp repeats and a VSG gene [40, 41]. Trypanosoma Human cases have reduced in recent years, currently brucei exhibits monoallelic expression of one ES at a at approximately 2000 cases per year, although under- time allowing the expression of one VSG variant per reporting and the discovery of asymptomatic carriers parasite [34, 42, 43]. ES transcription does not occur in [22] may require revaluation of the prospects for dis- the nucleolus, unlike other RNAP I transcripts (rRNA, ease elimination. For the animal disease, trypanosomosis procyclin genes [44, 45]), but at an extranucleolar focus remains prevalent and devastating, generating signifcant of RNAP I (the ‘expression site body’) [44, 46, 47]. Te restrictions on animal productivity in the tsetse belt of switch between diferent ES is controlled epigeneti- sub-Saharan Africa. cally [48] and occurs early during the time course of an Te genome of T. brucei has 11 megabase-chromo- infection [13, 39]. Later, but still early during the infec- somes (~of 35 Mb total) as well as 5 intermediate (200– tion, DNA recombination of entire VSG genes occurs 300 kb) and ~60–100 mini-chromosomes (30–150 kb) into the active ES, from mainly telomeric regions, and [23–25]. Te megabase chromosomes are segregated is mediated via the 70 bp repeats. When this repertoire via a kinetochore machinery that appears highly diver- is exhausted, recombination occurs from subtelomeric gent with respect to the canonical eukaryotic model array VSGs, with segmental VSGs conversion produc- [26]. Genes are organised and co-transcribed in large ing mosaic VSGs [13, 23, 39, 41, 49–51]. Tese VSG multi-gene (polycistronic) units [27]. Tere is little recombinations are dependent on a DNA break [40]. evidence of clustering of genes according to life-cycle Cytological organisation and fagellar motility have regulation in T. brucei, such that post transcriptional also proved fascinating areas of trypanosome biology of mechanisms control gene expression (RNA stability, relevance across eukaryotes. Trypanosomes are highly translation, codon usage) [18]. Most protein-coding ordered, with their single copy organelles precisely genes are transcribed by RNA polymerase II (RNAP positioned and their movements carefully orchestrated II) with the mRNA for all protein-coding genes being during cell division [52]. Ultrastructural studies using capped by addition via trans splicing of a 39 nt ‘spliced electron microscopy and electron tomography have leader’ (SL) sequence, this assisting translation and revealed how the microtubule
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