期刊论文详细信息
BMC Genomics
The wide expansion of hepatitis delta virus-like ribozymes throughout trypanosomatid genomes is linked to the spreading of L1Tc/ingi clade mobile elements
María Carmen Thomas2  Carlos Alonso1  Patricia Eugenia Carreira2  Manuel Carlos López2  Francisco José Sánchez-Luque2 
[1]Centro de Biología Molecular “Severo Ochoa”, CSIC-UAM, Campus Universidad Autónoma de Madrid, C/Nicolás Cabrera n°1, 28049 Madrid, Spain
[2]Instituto de Parasitología y Biomedicina “López-Neyra”, CSIC, Parque Tecnológico de Ciencias de la Salud, Av. del Conocimiento s/n, 18016 Granada, Spain
关键词: ingi;    SIDER;    L1Tc;    Leishmania;    Trypanosoma;    Pr77;    HDV-like ribozyme;    SINE;    LINE;    Retrotransposon;   
Others  :  1217258
DOI  :  10.1186/1471-2164-15-340
 received in 2013-11-28, accepted in 2014-04-24,  发布年份 2014
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【 摘 要 】

Background

Hepatitis Delta Virus (HDV)-like ribozymes have recently been found in many mobile elements in which they take part in a mechanism that releases intermediate RNAs from cellular co-transcripts. L1Tc in Trypanosoma cruzi is one of the elements in which such a ribozyme is located. It lies in the so-called Pr77-hallmark, a conserved region shared by retrotransposons belonging to the trypanosomatid L1Tc/ingi clade. The wide distribution of the Pr77-hallmark detected in trypanosomatid retrotransposons renders the potential catalytic activity of these elements worthy of study: their distribution might contribute to host genetic regulation at the mRNA level. Indeed, in Leishmania spp, the pervasive presence of these HDV-like ribozyme-containing mobile elements in certain 3′-untranslated regions of protein-coding genes has been linked to mRNA downregulation.

Results

Intensive screening of publicly available trypanosomatid genomes, combined with manual folding analyses, allowed the isolation of putatively Pr77-hallmarks with HDV-like ribozyme activity. This work describes the conservation of an HDV-like ribozyme structure in the Pr77 sequence of retrotransposons in a wide range of trypanosomatids, the catalytic function of which is maintained in the majority.

These results are consistent with the previously suggested common phylogenetic origin of the elements that belong to this clade, although in some cases loss of functionality appears to have occurred and/or perhaps molecular domestication by the host.

Conclusions

These HDV-like ribozymes are widely distributed within retrotransposons across trypanosomatid genomes. This type of ribozyme was once thought to be rare in nature, but in fact it would seem to be abundant in trypanosomatid transcripts. It can even form part of the pool of mRNA 3′-untranslated regions, particularly in Leishmania spp. Its putative regulatory role in host genetic expression is discussed.

【 授权许可】

   
2014 Sánchez-Luque et al.; licensee BioMed Central Ltd.

【 预 览 】
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【 参考文献 】
  • [1]Luan DD, Korman MH, Jakubczak JL, Eickbush TH: Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 1993, 72(4):595-605.
  • [2]Ohshima K, Okada N: SINEs and LINEs: symbionts of eukaryotic genomes with a common tail. Cytogenet Genome Res 2005, 110(1–4):475-490.
  • [3]Eickbush DG, Eickbush TH: R2 and R2/R1 hybrid non-autonomous retrotransposons derived by internal deletions of full-length elements. Mob DNA 2012, 3(1):10. BioMed Central Full Text
  • [4]Ullu E, Tschudi C: Alu sequences are processed 7SL RNA genes. Nature 1984, 312(5990):171-172.
  • [5]Wang H, Xing J, Grover D, Hedges DJ, Han K, Walker JA, Batzer MA: SVA elements: a hominid-specific retroposon family. J Mol Biol 2005, 354(4):994-1007.
  • [6]Gogolevsky KP, Vassetzky NS, Kramerov DA: 5S rRNA-derived and tRNA-derived SINEs in fruit bats. Genomics 2009, 93(5):494-500.
  • [7]Bringaud F, Berriman M, Hertz-Fowler C: Trypanosomatid genomes contain several subfamilies of ingi-related retroposons. Eukaryot cell 2009, 8(10):1532-1542.
  • [8]Smith M, Bringaud F, Papadopoulou B: Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome. BMC Genomics 2009, 10:240. BioMed Central Full Text
  • [9]Martin F, Maranon C, Olivares M, Alonso C, Lopez MC: Characterization of a non-long terminal repeat retrotransposon cDNA (L1Tc) from Trypanosoma cruzi: homology of the first ORF with the ape family of DNA repair enzymes. J Mol Biol 1995, 247(1):49-59.
  • [10]Kimmel BE, ole-MoiYoi OK, Young JR: Ingi, a 5.2-kb dispersed sequence element from Trypanosoma brucei that carries half of a smaller mobile element at either end and has homology with mammalian LINEs. Mol Cell Biol 1987, 7(4):1465-1475.
  • [11]Olivares M, Alonso C, López MC: The open reading frame 1 of the L1Tc retrotransposon of Trypanosoma cruzi codes for a protein with apurinic-apyrimidinic nuclease activity. J Biol Chem 1997, 272(44):25224-25228.
  • [12]Olivares M, García-Pérez JL, Thomas MC, Heras RS, López MC: The non-LTR retrotransposon L1Tc from Trypanosoma cruzi codes for a protein with RNase H activity. J Biol Chem 2002, 277(31):28025-28030.
  • [13]García-Pérez JL, González CI, Thomas MC, Olivares M, López MC: Characterization of the reverse transcriptase activity of the L1Tc retroelement from Trypanosoma cruzi. Cell Mol Life Sci 2003, 60(12):2692-2701.
  • [14]Heras S, López MC, García-Pérez JL, Martin S, Thomas MC: The L1Tc C-terminal domain from Trypanosoma cruzi non-LTR retrotransposon codes for a protein that bears two C2H2 zinc-finger motifs which is endowed with nucleic acid chaperone activity. Mol Cell Biol 2005, 25(21):9209-9220.
  • [15]Bringaud F, Garcia-Perez JL, Heras SR, Ghedin E, El-Sayed NM, Andersson B, Baltz T, Lopez MC: Identification of non-autonomous non-LTR retrotransposons in the genome of trypanosoma cruzi. Mol Biochem Parasitol 2002, 124(1–2):73-78.
  • [16]Hasan G, Turner MJ, Cordingley JS: Complete nucleotide sequence of an unusual mobile element from trypanosoma brucei. Cell 1984, 37(1):333-341.
  • [17]Bringaud F, Ghedin E, Blandin G, Bartholomeu DC, Caler E, Levin MJ, Baltz T, El-Sayed NM: Evolution of non-LTR retrotransposons in the trypanosomatid genomes: Leishmania major has lost the active elements. Mol Biochem Parasitol 2006, 145(2):158-170.
  • [18]Swergold GD: Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol 1990, 10(12):6718-6729.
  • [19]Contursi C, Minchiotti G, Di Nocera PP: Identification of sequences which regulate the expression of Drosophila melanogaster Doc elements. J Biol Chem 1995, 270(44):26570-26576.
  • [20]McLean C, Bucheton A, Finnegan DJ: The 5′ untranslated region of the I factor, a long interspersed nuclear element-like retrotransposon of Drosophila melanogaster, contains an internal promoter and sequences that regulate expression. Mol Cell Biol 1993, 13(2):1042-1050.
  • [21]Zhou J, Eickbush TH: The pattern of R2 retrotransposon activity in natural populations of Drosophila simulans reflects the dynamic nature of the rDNA locus. PLoS Genet 2009, 5(2):e1000386.
  • [22]Eickbush TH: R2 and Related site-specific non-long terminal repeat retrotransposons. In Mobile DNA II. Edited by Craig NL, Craigie R, Gellert M, Lambowitz AM. Washington, DC: ASM Press; 2002:813-835.
  • [23]Eickbush DG, Eickbush TH: R2 retrotransposons encode a self-cleaving ribozyme for processing from an rRNA cotranscript. Mol Cell Biol 2010, 30(13):3142-3150.
  • [24]Ruminski DJ, Webb CH, Riccitelli NJ, Luptak A: Processing and translation initiation of non-long terminal repeat retrotransposons by hepatitis delta virus (HDV)-like self-cleaving ribozymes. J Biol Chem 2011, 286(48):41286-41295.
  • [25]Sanchez-Luque FJ, Lopez MC, Macias F, Alonso C, Thomas MC: Identification of an hepatitis delta virus-like ribozyme at the mRNA 5′-end of the L1Tc retrotransposon from Trypanosoma cruzi. Nucleic Acids Res 2011, 39(18):8065-8077.
  • [26]Eickbush DG, Burke WD, Eickbush TH: Evolution of the r2 retrotransposon ribozyme and its self-cleavage site. PLoS One 2013, 8(9):e66441.
  • [27]Salehi-Ashtiani K, Luptak A, Litovchick A, Szostak JW: A genomewide search for ribozymes reveals an HDV-like sequence in the human CPEB3 gene. Science (New York, NY) 2006, 313(5794):1788-1792.
  • [28]Webb CH, Riccitelli NJ, Ruminski DJ, Luptak A: Widespread occurrence of self-cleaving ribozymes. Science (New York, NY) 2009, 326(5955):953.
  • [29]Heras SR, Lopez MC, Olivares M, Thomas MC: The L1Tc non-LTR retrotransposon of Trypanosoma cruzi contains an internal RNA-pol II-dependent promoter that strongly activates gene transcription and generates unspliced transcripts. Nucleic Acids Res 2007, 35(7):2199-2214.
  • [30]Sanchez-Luque F, Lopez MC, Macias F, Alonso C, Thomas MC: Pr77 and L1TcRz: a dual system within the 5′-end of L1Tc retrotransposon, internal promoter and HDV-like ribozyme. Mob Genet Elements 2012, 2(1):1-7.
  • [31]Martinez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K, Myler PJ: Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 2003, 11(5):1291-1299.
  • [32]Siegel TN, Hekstra DR, Kemp LE, Figueiredo LM, Lowell JE, Fenyo D, Wang X, Dewell S, Cross GA: Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev 2009, 23(9):1063-1076.
  • [33]Bringaud F, Muller M, Cerqueira GC, Smith M, Rochette A, El-Sayed NM, Papadopoulou B, Ghedin E: Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog 2007, 3(9):1291-1307.
  • [34]Muller M, Padmanabhan PK, Papadopoulou B: Selective inactivation of SIDER2 retroposon-mediated mRNA decay contributes to stage- and species-specific gene expression in Leishmania. Mol Microbiol 2010, 77(2):471-491.
  • [35]Muller M, Padmanabhan PK, Rochette A, Mukherjee D, Smith M, Dumas C, Papadopoulou B: Rapid decay of unstable Leishmania mRNAs bearing a conserved retroposon signature 3′-UTR motif is initiated by a site-specific endonucleolytic cleavage without prior deadenylation. Nucleic Acids Res 2010, 38(17):5867-5883.
  • [36]Lyons AJ, Robertson HD: Detection of tRNA-like structure through RNase P cleavage of viral internal ribosome entry site RNAs near the AUG start triplet. J Biol Chem 2003, 278(29):26844-26850.
  • [37]Bringaud F, Berriman M, Hertz-Fowler C: TSIDER1, a short and non-autonomous Salivarian trypanosome-specific retroposon related to the ingi6 subclade. Mol Biochem Parasitol 2011, 179(1):30-36.
  • [38]Requena JM, Folgueira C, Lopez MC, Thomas MC: The SIDER2 elements, interspersed repeated sequences that populate the Leishmania genomes, constitute subfamilies showing chromosomal proximity relationship. BMC Genomics 2008, 9:263. BioMed Central Full Text
  • [39]Fraga J, Montalvo AM, De Doncker S, Dujardin JC, Van der Auwera G: Phylogeny of Leishmania species based on the heat-shock protein 70 gene. Infect Genet Evol 2010, 10(2):238-245.
  • [40]Requena JM, Chicharro C, Garcia L, Parrado R, Puerta CJ, Canavate C: Sequence analysis of the 3′-untranslated region of HSP70 (type I) genes in the genus Leishmania: its usefulness as a molecular marker for species identification. Parasit Vectors 2012, 5:87. BioMed Central Full Text
  • [41]Kuo MY, Sharmeen L, Dinter-Gottlieb G, Taylor J: Characterization of self-cleaving RNA sequences on the genome and antigenome of human hepatitis delta virus. J Virol 1988, 62(12):4439-4444.
  • [42]Chadalavada DM, Cerrone-Szakal AL, Bevilacqua PC: Wild-type is the optimal sequence of the HDV ribozyme under cotranscriptional conditions. RNA (New York, NY) 2007, 13(12):2189-2201.
  • [43]Shimamura M, Yasue H, Ohshima K, Abe H, Kato H, Kishiro T, Goto M, Munechika I, Okada N: Molecular evidence from retroposons that whales form a clade within even-toed ungulates. Nature 1997, 388(6643):666-670.
  • [44]Nikaido M, Rooney AP, Okada N: Phylogenetic relationships among cetartiodactyls based on insertions of short and long interpersed elements: hippopotamuses are the closest extant relatives of whales. Proc Natl Acad Sci U S A 1999, 96(18):10261-10266.
  • [45]van Tol H, Buzayan JM, Feldstein PA, Eckstein F, Bruening G: Two autolytic processing reactions of a satellite RNA proceed with inversion of configuration. Nucleic Acids Res 1990, 18(8):1971-1975.
  • [46]Sharmeen L, Kuo MY, Dinter-Gottlieb G, Taylor J: Antigenomic RNA of human hepatitis delta virus can undergo self-cleavage. J Virol 1988, 62(8):2674-2679.
  • [47]Kibbe WA: OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 2007, 35(Web Server issue):W43-W46.
  • [48]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 2007, 23(21):2947-2948.
  • [49]Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O: Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, 36(Web Server issue):W465-W469.
  • [50]Dereeper A, Audic S, Claverie JM, Blanc G: BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 2010, 10:8. BioMed Central Full Text
  • [51]Harrison CJ, Langdale JA: A step by step guide to phylogeny reconstruction. Plant J 2006, 45:561-572.
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