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Diversity and Functional Plasticity of Eukaryotic Selenoproteins: Identification and Characterization of the Selj Family

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Diversity and Functional Plasticity of Eukaryotic Selenoproteins: Identification and Characterization of the Selj Family Diversity and functional plasticity of eukaryotic selenoproteins: Identification and characterization of the SelJ family Sergi Castellano*†, Alexey V. Lobanov‡, Charles Chapple*, Sergey V. Novoselov‡, Mario Albrecht§, Deame Hua‡, Alain Lescure¶, Thomas Lengauer§, Alain Krol¶, Vadim N. Gladyshev‡, and Roderic Guigo´ * *Grup de Recerca en Informa`tica Biome`dica, Institut Municipal d’Investigacio´Me` dica, Universitat Pompeu Fabra and Centre de Regulacio´Geno`mica, Carrer del Doctor Aiguader 80, 08003 Barcelona, Spain; ‡Department of Biochemistry, University of Nebraska, Lincoln, NE 65588; §Max Planck Institute for Informatics, Stuhlsatzenhausweg 85, 66123 Saarbru¨cken, Germany; and ¶Institut de Biologie Mole´culaire et Cellulaire, 15 Rue Rene´Descartes, 67084 Strasbourg Cedex, France Edited by Philip P. Green, University of Washington School of Medicine, Seattle, WA, and approved September 22, 2005 (received for review June 19, 2005) Selenoproteins are a diverse group of proteins that contain sel- evolutionary direction (if any) of Sec͞Cys interconversion. This enocysteine (Sec), the 21st amino acid. In the genetic code, UGA distribution of Sec and Cys residues across genomes hinders the serves as a termination signal and a Sec codon. This dual role has identification of true Sec-containing proteins. precluded the automatic annotation of selenoproteins. Recent In consequence, the description of eukaryotic selenoproteomes advances in the computational identification of selenoprotein is incomplete. The number, functional diversity, and phylogenetic genes have provided a first glimpse of the size, functions, and distribution of eukaryotic selenoproteins are poorly known and, phylogenetic diversity of eukaryotic selenoproteomes. Here, we thus, the importance of Sec and selenium in protein function and describe the identification of a selenoprotein family named SelJ. In evolution remains unclear, despite an increasing body of evidence contrast to known selenoproteins, SelJ appears to be restricted to linking selenium deficiency to a number of pathologies (reviewed actinopterygian fishes and sea urchin, with Cys homologues only in ref. 17). Recently, computational approaches have been devel- found in cnidarians. SelJ shows significant similarity to the jellyfish oped that have greatly contributed to the characterization of J1-crystallins and with them constitutes a distinct subfamily within selenoproteins in many eukaryotic genomes. Specific methods have the large family of ADP-ribosylation enzymes. Consistent with its been developed to predict SECIS elements in nucleotide sequences potential role as a structural crystallin, SelJ has preferential and (5, 6). SECIS predictions, in turn, have been used to instruct homogeneous expression in the eye lens in early stages of ze- modified gene prediction algorithms to ignore UGA codons as brafish development. A structural role for SelJ would be in contrast terminators in putative exon sequences when SECIS elements are to the majority of known selenoenzymes. The unusually highly predicted at the appropriate distance (7–9). In addition, compar- restricted phylogenetic distribution of SelJ, its specialization, and ative sequence analysis methods have proven to be very powerful the comparative analysis of eukaryotic selenoproteomes reveal the in uncovering novel selenoproteins. Indeed, protein sequence con- diversity and functional plasticity of selenoproteins and point to a servation across a TGA codon between sequences from species at mosaic evolution of the use of Sec in proteins. large phylogenetic distances is strongly indicative of the Sec coding function (10). ͉ ͉ ͉ ADP-ribosylation J1-crystallins selenocysteine selenium Here, we report the discovery by computational and experi- mental means of a selenoprotein family designated SelJ in the elenocysteine (Sec) residues are found only in a small group of genome of Tetraodon nigroviridis. SelJ has a very restricted Sproteins called selenoproteins. Selenoproteins with character- phylogenetic distribution and, in contrast to all known eukary- ized functions are enzymes involved in redox reactions. Sec is otic selenoproteins, does not exist in mammalian genomes, not inserted by dynamic recoding of an in-frame UGA stop codon even as a Cys homologue. In addition, although the majority of located upstream of the actual termination codon (1). Selenopro- selenoproteins are assumed to have enzymatic functions, com- teins are present in eukaryotes and prokaryotes and, although their putational and experimental data suggest that SelJ could have a sets of selenoproteins (selenoproteomes) do not completely overlap structural role. Comparison of eukaryotic selenoproteomes (2), their intersection appears to be larger than previously thought highlights the scattered phylogenetic distribution of selenopro- (3). In eukaryotes, the Sec insertion sequence (SECIS), an RNA teins, arguing for a mosaic evolution of specialized proteins in Ј stem-loop located in the 3 UTR of selenoprotein genes, recruits which the differential use of Sec and Cys shapes the size and several transacting factors to recode UGA from termination to Sec function of eukaryotic selenoproteomes. insertion (4). The dual function of this codon confounds gene- finding programs and human curators, making selenoprotein iden- Methods tification a challenge (5–10). Gene and SECIS Prediction. The T. nigroviridis sequence data (18) was In addition, Cys and Sec are structurally related amino acids, with screened for previously uncharacterized selenoprotein genes using Sec incorporating selenium in the position of sulfur in Cys. The three independent computational methods (see Supporting Meth- functional resemblance of Sec and Cys is supported by the obser- vation that their residues occupy equivalent positions in homolo- gous proteins. As expected, mutation of the Sec residue to Cys Conflict of interest statement: No conflicts declared. results in variants that are active but have a lower catalytic efficiency This paper was submitted directly (Track II) to the PNAS office. (11–13), although they may have an enhanced translation (13). Abbreviations: Sec, selenocysteine; SECIS, Sec insertion sequence; ARH, ADP-ribosylglyco- Furthermore, natural Cys-containing counterparts are usually in- hydrolase; mjARH, ARH from Methanococcus jannaschii. ferior catalysts (14, 15), but similar reactivity has also been reported See Commentary on page 16123. (16). Hence, Sec, per se, does not possess an essential role in protein †To whom correspondence should be sent at the present address: Department of Molecular function and these two residues seem to be partially interchange- Biology and Genetics, Cornell University, 101 Biotechnology Building, Ithaca, NY 14853. able. Accordingly, Sec and Cys residues are alternatively found in E-mail: [email protected]. orthologous proteins in different species raising the issue of the © 2005 by The National Academy of Sciences of the USA 16188–16193 ͉ PNAS ͉ November 8, 2005 ͉ vol. 102 ͉ no. 45 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0505146102 Downloaded by guest on September 26, 2021 SEE COMMENTARY Fig. 1. SelJ gene and SECIS struc- ture. (A) SelJ gene structure in T. ni- groviridis. Coding exon regions are shown in blue. The annotated gene in Ensembl (GSTENG00015130001) has the frame changed and uses a different termination codon. There- fore, SelJ is reannotated with the Sec codon (TGA in the genomic se- quence) and the SECIS element in the noncoding region of the last exon. (B) SelJ SECIS element. ods, which is published as supporting information on the PNAS web ACCTGCGGTTTGCCTGGTGC-3Ј and 5Ј-GGAATGCACC- site). The SelJ (Fig. 1A) selenoprotein mRNA was found through AGGCAAACCGCAGGTATTTGGAAA-3Ј primers and a a coordinated prediction of ORFs interrupted by in-frame UGA QuikChange Mutagenesis kit (Stratagene). The coding region of codons in cDNA sequences with the gene prediction program the resulting Cys mutant of SelJ was amplified with 5Ј-TCGA- GENEID (19) and SECIS elements (Fig. 1B) with SECISEARCH (8, 9). TCTCGAGGATTTCAAGATGGCTCTTGC-3Ј and 5Ј-CTAA- GGAATCCCTTGTTTTTCCAGGAAGGTGGAATC-3Ј and 75Se Labeling. The partial sequence of the zebrafish SelJ cDNA that cloned upstream of GFP in pEGFP-N2 vector by using EcoR I and included a region coding for a 18-kDa C-terminal portion of the XhoI restriction sites. NIH 3T3 cells were transfected as described protein and the 3Ј UTR with a predicted SECIS element was above, and fluorescence was detected with an Olympus FV500 amplified with 5Ј-AGTCGCTCGAGGTTGAAGAAGCAGTC- confocal microscope at the Microscopy Core Facility at the Uni- CGTGTCAC-3Ј and 5Ј-GCTTGGGATCCATTTTCCGCATGT- versity of Nebraska, Lincoln (see Fig. 3). CATGCTG-3Ј primers and cloned into pEGFP-C3 (Clontech) vector by using XhoI and BamHI restriction sites to generate the Homology Searches. TBLASTN (20) was used to query the following GFP–SelJ construct, which codes for a fusion protein containing for SelJ homologues: the National Center for Biotechnology In- GFP followed by a C-terminal region of SelJ. The plasmid was formation (NCBI, www.ncbi.nlm.nih.gov) collection of 62 eukary- purified with an EndoFree Maxi kit (Qiagen, Valencia, CA). NIH otic (partial and complete), 25 archaeal, and 354 bacterial genomes, 3T3 cells were transfected with the GFP–SelJ construct using the NCBI eukaryotic ESTs, and sets of eukaryotic transcripts (81 Lipofectamine and Plus reagents (Invitrogen). Transfected cells species) for SelJ homologues from The Institute for Genomic were supplemented with 5–10
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