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Transcription in Kinetoplastid Protozoa: Why Be Normal? David A

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Transcription in Kinetoplastid Protozoa: Why Be Normal? David A Microbes and Infection 5 (2003) 1231–1240 www.elsevier.com/locate/micinf Review Transcription in kinetoplastid protozoa: why be normal? David A. Campbell *, Sean Thomas, Nancy R. Sturm Department of Microbiology, Immunology and Molecular Genetics, University of California at Los Angeles, 609 Charles E. Young Drive East, Los Angeles, CA 90095-1489, USA Abstract Transcription in the kinetoplastid protozoa shows substantial variation from the paradigms of eukaryotic gene expression, including polycistronic transcription, a paucity of RNA polymerase (RNAP) II promoters, no qualitative regulated transcription initiation for most protein-coding genes, transcription of some protein-coding genes by RNAP I, an exclusive subnuclear location for VSG transcription, the dependence of small nuclear RNA gene transcription on an upstream tRNA gene, and the synthesis of mitochondrial tRNAs in the nucleus. Here, we present a broad overview of what is known about transcription in the kinetoplastids and what has yet to be determined. © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Leishmania; Polycistronic; Promoter; Transcription factor; trans splicing; Trypanosoma 1. Introduction mastigote stage [1]. Transcriptional rates through a polycis- tron do not appear to vary greatly, and protein levels may be The order kinetoplastida contains important pathogens of determined very crudely by gene copy number. A feature of livestock, humans and plants (Trypanosoma, Leishmania the kinetoplastid genome is that genes for many abundant and Phytomonas). These unicellular organisms represent an proteins are found in multicopy tandem arrays. Post- early branch in the eukaryotic evolutionary tree and possess a transcriptional events, such as mRNA processing and stabil- plethora of biochemical, genetic and morphological features ity, are among the varied mechanisms for differential control that are either unique to the group (e.g. mitochondrial of protein levels in this group of organisms [2]. Nevertheless, minicircles, uridine insertion/deletion editing, and glyco- kinetoplastid protozoa possess a variety of non-standard somes) or that are used to a greater extent than in most other mechanisms for the synthesis of different RNA molecules organisms (e.g. glucosyl phosphatidylinositol (GPI) anchor- (Fig. 1). Unexpected transcriptional features were first en- ing of membrane proteins, bent DNA, polycistronic tran- countered in Trypanosoma brucei, where VSG mRNA was scription, trans splicing, and fragmented rRNA). From a shown to be synthesized by an a-amanitin-insensitive RNA standpoint of cellular differentiation, these diverse protozoa polymerase (RNAP) [3]. It was a further curiosity that differ- range from free-living cells that are capable of encystation to ent VSG mRNAs had the same 5′-end sequence, which was forms that are dependent on one or two host organisms. not found in the gene. This sequence became known as the These developmental stages display distinct morphologic spliced leader (SL, a.k.a. miniexon) and was ultimately and metabolic characteristics consistent with a highly regu- found to be present at the 5′-end of all mRNAs [4]. The SL lated level of differential protein expression. was synthesized by an a-amanitin-sensitive RNAP [5], indi- Unlike most other organisms, this regulation is not deter- cating the synthesis of a single mRNA by two distinct mined qualitatively at the level of transcription initiation, RNAPs. Furthermore, the SL and VSG exons originated with the exception of a set of variant surface glycoprotein from two different chromosomes. Joining of the two distinct (VSG) genes expressed exclusively in the metacyclic trypo- exons is achieved by trans splicing [6]. The necessity for trans splicing is now appreciated as the mechanism for ma- Abbreviations: ESB, expression site body; GRNA, guide RNA; J, b-D- glucosyl-hydroxymethyluracil; M7G, 7-methyl guanosine; RNAP, RNA po- turing the pre-mRNAs generated by polycistronic transcrip- lymerase; SL, spliced leader; SnRNA, small nuclear RNA; SnoRNA, small tion of VSG [7] and a-amanitin-sensitive housekeeping nucleolar RNA; TBP,TATA-binding protein;VSG, variant surface glycopro- genes [8]. By this process, the mature mRNA obtains a tein. 7-methyl guanosine (m7G) cap from the SL RNA as well as a * Corresponding author. Tel.: +1-310-206-5556; fax: +1-310-206-5231. poly-A tail in a coupled process [9]. E-mail address: [email protected] (D.A. Campbell). © 2003 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. doi:10.1016/j.micinf.2003.09.005 1232 D.A. Campbell et al. / Microbes and Infection 5 (2003) 1231–1240 Fig. 1. The spectrum of kinetoplastid transcription. Superimposed on a promastigote form is a wheel of nuclear transcription with the three classes of RNAP, I (yellow), II (red) and III (blue) shown in the center. The transcription of different classes of genes is indicated as the outer edge overlapping the different classes of RNAP. The synthesis of distinct classes of RNAs by different RNAPs is indicated by blended colours: protein-coding mRNA (orange), snRNAs (purple) and rRNA (green). tRNA synthesized in the nucleus is trafficked through the cytosol to the mitochondrion. In the mitochondrion, transcription of mRNA, rRNA and gRNA is performed by at least one nuclear-encoded mitochondrial RNAP. Maturation of nuclear and mitochondrial mRNA by trans splicing or RNA editing is indicated. The extent to which polycistronic transcription occurs in 2. Basal transcription the kinetoplastids is evident from the diametric structure of chromosome 1 in Leishmania major, where 50 adjacent open There is increasing experimental and bioinformatic evi- reading frames (ORFs) are oriented unidirectionally on one dence for conservation of the eukaryotic basal transcription strand and the remaining 29 ORFs on the opposite strand [10] machinery and signals in the kinetoplastid protozoa. Of the (see Ref. [11] for the structure of other Leishmania chromo- synthetic machinery, the standard four classes of RNAP have somes). A rationale for gene order in the kinetoplastids is not been identified in the kinetoplastid protozoa. The three evident. With a few exceptions, such as the pyrimidine biosyn- classes of eukaryotic nuclear RNAP (I, II and III) have been thetic gene cluster [12], kinetoplastid polycistrons do not identified by chromatography and largest-polypeptide sub- appear to encode functionally related proteins as found in unit composition [19]. A summary of the known core nuclear bacterial and nematode operons [13]. It is possible that a high promoter structures and interacting factors is shown in Fig. 3. rate of recombination among chromosomes in the kinetoplas- Furthermore, a mitochondrial RNAP has been identified that tids has resulted in the shuffling of the gene order. A schematic generates mRNAs from the maxicircle DNA [20]. of discontinuous transcription and the production of mature The conservation of cis signals is evident in genes for mRNA by trans splicing is presented in Fig. 2. The recent small RNAs in kinetoplastids. Consensus internal promoter evidence for transcription initiation by RNAP II in the elements for RNAP III have been identified in 5S rRNA and strand-switch region of L. major chromosome 1 [14] will tRNA genes [21,22], as has a conserved external element for resolve the hunt for this elusive event, but does not necessarily RNAP II-transcribed small nuclear RNA (snRNA) genes eliminate the possibility of low background levels of non- upstream of the SL RNA gene [23]. The biochemical charac- specific transcription of protein-coding genes by RNAP II. terization of trans-acting proteins that bind to the promoter Here, we summarize the current state of knowledge on elements is in its early stages. There is a remarkable dearth of kinetoplastid transcription in general and emphasize new orthologous transcription factors in the kinetoplastid data- developments and transcriptional strategies that are unique to bases [24]. Nonetheless, a conserved subunit of the general the trypanosomes. Previous detailed reviews of topics in transcription factors for all three RNAPs [25], the TATA-box- kinetoplastid gene expression [15–18] cite many of the origi- binding protein (TBP), was revealed in genome sequencing nal research publications that are omitted here due to space projects from multiple kinetoplastid species (e.g. T. brucei limitations. AQ947932). D.A. Campbell et al. / Microbes and Infection 5 (2003) 1231–1240 1233 Fig. 2. Schematic of discontinuous transcription and the production of mature mRNA by trans splicing. Transcription of short discrete tandemly repeated genes (SL RNA) and polycistronic protein-coding regions (exemplified by L. major chromosome 1 [10]) by RNAP II is indicated at the left. The primary transcripts from the two classes of gene are shown in the center intersecting with steps in the trans splicing pathway (right panel). The bimolecular trans splicing reaction resembles the unimolecular cis splicing pathway in many aspects, including the initial cleavage of the SL RNA splice donor site, the formation of 5′–2′ phosphodiester bond on a branch-point A residue, cleavage at the pre-mRNA splice acceptor site and ligation of the two exons. Differences between the two processes include the formation of a Y-branched intermediate (rather that a lariat-like intermediate) and the coupled polyadenylation of the upstream mRNA. Fig. 3. The structure of promoter elements and transcription units in representative kinetoplastid protozoa.
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