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Functions and Cellular Localization of Cysteine Desulfurase And Functions and cellular localization of cysteine desulfurase and selenocysteine lyase in Trypanosoma brucei Pavel Poliak1, Douglas Van Hoewyk2, Miroslav Obornı´k1, Alena Zı´kova´ 1,3, Kenneth D. Stuart3, Jan Tachezy4, Marinus Pilon5 and Julius Lukesˇ 1 1 Biology Centre, Institute of Parasitology and Faculty of Science, University of South Bohemia, Cˇ eske´ Budeˇ jovice (Budweis), Czech Republic 2 Department of Biology, Coastal Carolina University, Conway, SC, USA 3 Seattle Biomedical Research Institute, Seattle, WA, USA 4 Department of Parasitology, Charles University, Prague, Czech Republic 5 Biology Department, Colorado State University, Fort Collins, CO, USA Keywords Nfs-like proteins have cysteine desulfurase (CysD) activity, which removes Fe–S cluster; mitochondrion; RNAi; sulfur (S) from cysteine, and provides S for iron–sulfur cluster assembly selenoprotein; Trypanosoma and the thiolation of tRNAs. These proteins also have selenocysteine lyase activity in vitro, and cleave selenocysteine into alanine and elemental sele- Correspondence J. Lukesˇ, Institute of Parasitology, nium (Se). It was shown previously that the Nfs-like protein called Nfs Branisˇovska´ 31, 37005 Cˇ eske´ Budeˇ jovice, from the parasitic protist Trypanosoma brucei is a genuine CysD. A second Czech Republic Nfs-like protein is encoded in the nuclear genome of T. brucei. We called Fax: + 420 38 531 0388 this protein selenocysteine lyase (SCL) because phylogenetic analysis Tel: + 420 38 777 5416 reveals that it is monophyletic with known eukaryotic selenocysteine lyases. E-mail: [email protected] The Nfs protein is located in the mitochondrion, whereas the SCL protein seems to be present in the nucleus and cytoplasm. Unexpectedly, downre- (Revised 22 July 2009, revised 5 November 2009, accepted 9 November 2009) gulation of either Nfs or SCL protein leads to a dramatic decrease in both CysD and selenocysteine lyase activities concurrently in the mitochondrion doi:10.1111/j.1742-4658.2009.07489.x and the cytosolic fractions. Because loss of Nfs causes a growth phenotype but loss of SCL does not, we propose that Nfs can fully complement SCL, whereas SCL can only partially replace Nfs under our growth conditions. Structured digital abstract l MINT-7298305: NFS (uniprotkb:Q386Y7) and PHB1 (uniprotkb:Q57UX1) colocalize (MI:0403) by cosedimentation through density gradients (MI:0029) l MINT-7298357: SCL (uniprotkb:Q38DC4) and Enolase (uniprotkb:Q38BV6) colocalize (MI:0403) by cosedimentation through density gradients (MI:0029) Introduction Nfs-like proteins have cysteine desulfurase (CysD) (termed NifS, IscS, CsdA or SufS in bacteria, depend- activity, and were first discovered in the nitrogen-fixing ing on the gene clusters in which they are found and microbe Azotobacter vinelandii, where they are dedi- Nfs in mitochondria) that provide the S for Fe–S clus- cated to the assembly of the iron–sulfur (Fe–S) clusters ters. Eukaryotic Nfs proteins have a stably interacting of nitrogenase [1]. These pyridoxal 5-phosphate-depen- partner Isd11, which is required for their function dent proteins catalyze conversion of the amino acid [2–4], and transiently interact with the scaffold protein cysteine into alanine and elemental sulfur (S) [1]. All IscU, upon which the clusters are formed [5]. Thus, organisms studied to date encode homologues of Nfs the Nfs protein has a central and conserved function Abbreviations CysD, cysteine desulfurase; GAP1, guide RNA-binding protein 1; HA, hemagglutinin; SCL, selenocysteine lyase. FEBS Journal 277 (2010) 383–393 ª 2009 The Authors Journal compilation ª 2009 FEBS 383 Trypanosoma brucei selenocystein lyase P. Poliak et al. in the assembly of Fe–S clusters [6,7]. In every pro- Nfs-like proteins [20]. Downregulation of the Nfs pro- karyotic and eukaryotic cell, these ancient and omni- tein, which is confined to the mitochondrion, impaired present cofactors are subsequently incorporated into ATP production, cellular respiration and growth, sug- dozens of Fe–S proteins. These Fe–S proteins are best gesting that this protein is essential for the assembly of known for their vital role in the redox reactions during Fe–S clusters incorporated into the mitochondrial mitochondrial electron transport, but also have a simi- proteins [20]. More recently, it was discovered that in lar function in photosynthesis [8], the formation of trypanosomes ablated for Nfs, tRNA thiolation is biotin and thiamine, gene expression and other cellular disrupted [21]. Moreover, in Saccharomyces cerevisiae processes [6,7]. and T. brucei, the mitochondrially located Nfs1 and Moreover, many organisms contain more than one Nfs proteins, respectively, are responsible for the thio- Nfs-like protein. For example, Escherichia coli contains lation of tRNAs in both the mitochondria and cyto- three distinct Nfs-like proteins (IscS, CsdA and SufS). plasm [21,22]. Because T. brucei contains a set of Although the role of CsdA in E. coli is not fully selenoproteins [23–25], as well as a complete machinery understood, IscS seems to have a general housekeeping for the formation of Sec–tRNASec [26], we undertook role, and SufS is thought to function during oxidative functional characterization of cells with downregulated stress [9]. The model plant Arabidopsis thaliana also Nfs-like protein of the selenocysteine type. encodes three functionally distinct Nfs-like proteins localized to the chloroplast, mitochondria and cytosol Results [10]. Two Nfs-like proteins have been identified in the apicomplexan protist Plasmodium [11], including one Phylogenetic analysis localized to the apicoplast, whereas the yeast and human genomes encode only a single Nfs-like protein. A genome-wide search revealed that T. brucei and all However, the human NFS1 gene contains an alterna- other kinetoplastid flagellates, for which full genome tive start site, which provides dual localization of the sequences are available, contain two Nfs-like proteins protein to the mitochondria or the cytosol and nucleus in their nuclear genome. Recent evidence suggests that [12]. In similar fashion, the yeast Nfs1 protein is pre- one of them, called Nfs (formerly TbIscS2), exhibits dominantly found in the mitochondion, but is also CysD activity and has a function in Fe–S cluster localized to the nucleus in small amounts, and has assembly similar to other well-studied homologues been shown to be indispensable for survival [13,14]. found in eukaryotes [20]. The second gene codes for a Yeast is not dependent on mitochondrial electron 451 amino acid protein with calculated molecular mass transport during anaerobic growth and so it is likely of 48.9 kDa. It contains a highly conserved PLP-bind- that the yeast Nfs1 protein is essential because of the ing lysine 258, the active cysteine 393 responsible for Fe–S cluster assembly for proteins localized in the desulfuration, as well as histidine 125, which initiates cytosol and the nucleus. Moreover, yeast Nfs1 is also the release of sulfur by deprotonation of l-cysteine. In necessary for the thiolation of tRNAs [15]. Indeed, the sequence, however, the conserved serine 255 is mutation of the nuclear localization signal in the replaced by cysteine, and a substantial part of the mature Nfs1 protein is also lethal in yeast, despite hav- active site loop, as well as the C-terminal region ing no effect on mitochondrial Fe–S proteins. These known to mediate interaction with IscU, are lacking. results suggest that the yeast Nfs1 protein has an A predicted nuclear localization signal (PPLKKLR) is essential role in both nuclear and cytosolic Fe–S clus- located in the N-terminal region of the protein ter assembly [15]. sequence. Interestingly, in addition to CysD activity, all Nfs- We have performed an extensive phylogenetic anal- like proteins have selenocysteine lyase (SCL) activity, ysis of Nfs-like genes from T. brucei using maximum which cleaves selenocysteine into alanine and selenium. likelihood, maximum parsimony and neighbor joining [16]. SCL activity is essential for organisms that analyses (see Experimental procedures for details). An require selenium, as first documented in bacteria and unrooted phylogenetic tree obtained from an align- later in mammals, both of which contain selenopro- ment of amino acid sequences of the Nfs ⁄ IscS and teins [17]. Single-celled organisms, such as the green SCL genes from 90 prokaryotes and 60 eukaryotes algae Chlamydomonas reinhardtii and Emiliana huxleyi revealed a very distant position for both T. brucei are also known to contain selenoproteins [18], genes (Fig. 1). The analysis did not recover a single although their set is smaller than in mammals [19]. clade containing solely prokaryotic sequences, but The genome of Trypanosoma brucei, the causative rather several paraphyletic clades. Eukaryotic genes agent of African sleeping sickness, encodes two are split into two large groups of different origin, 384 FEBS Journal 277 (2010) 383–393 ª 2009 The Authors Journal compilation ª 2009 FEBS P. Poliak et al. Trypanosoma brucei selenocystein lyase 84/dt/64 Ricinus communis 90/64/61 Arabidopsis thaliana 98/65/83 Oryza sativa Physcomitrella patens Ostreococcus tauri Ostreococcus lucimarinus 68/67/- Chlamydomonas reinhardtii 83/56/84 Leishmania infantum Leishmania major Leishmania braziliensis Trypanosoma cruzi Trypanosoma brucei NfS 99/79/96 Rattus norvegicus Mus musculus 62/91/- Homo sapiens 65/dt/- Drosophila melanogaster Caenorhabditis elegans Dictyostelium discoideum Cyanidioschyzon merolae Thalassiosira pseudonana 58-/- Phaeodactylum tricornutum
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