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An Unusual Primate Locus That Attracted Two Independent Alu Insertions and Facilitates Their Transcription

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An Unusual Primate Locus That Attracted Two Independent Alu Insertions and Facilitates Their Transcription doi:10.1016/j.jmb.2005.03.058 J. Mol. Biol. (2005) 350, 200–214 An Unusual Primate Locus that Attracted Two Independent Alu Insertions and Facilitates their Transcription A. Ludwig, T. S. Rozhdestvensky, V. Yu. Kuryshev, J. Schmitz and J. Brosius* Institute of Experimental BC200 RNA, a neuronal, small non-messenger RNA that originated from a Pathology, ZMBE, University of monomeric Alu element is specific to anthropoid primates. Tarsiers lack an Mu¨nster, Von-Esmarch-Str. 56 insert at the orthologous genomic position, whereas strepsirrhines D-48149 Mu¨nster, Germany (Lemuriformes and Lorisiformes) acquired a dimeric Alu element, independently from anthropoids. In Galago moholi, the CpG dinucleotides are conspicuously conserved, while in Eulemur coronatus a large proportion is changed, indicating that the G. moholi Alu is under purifying selection and might be transcribed. Indeed, Northern blot analysis of total brain RNA from G. moholi with a specific probe revealed a prominent signal. In contrast, a corresponding signal was absent from brain RNA from E. coronatus. Isolation and sequence analysis of additional strepsirrhine loci confirmed the differential sequence conservation including CpG patterns of the orthologous dimeric Alu elements in Lorisiformes and Lemuriformes. Interestingly, all examined Alu elements from Lorisiformes were transcribed, while all from Lemuriformes were silent when transiently transfected into HeLa cells. Upstream sequences, especially those between the transcriptional start site and K22 upstream, were important for basal transcriptional activity. Thus, the BC200 RNA gene locus attracted two independent Alu insertions during its evolutionary history and provided upstream promoter elements required for their transcription. q 2005 Elsevier Ltd. All rights reserved. Keywords: small non-messenger RNA; Alu elements; primate evolution; *Corresponding author retronuons; neuronal transcription Introduction DNA sequences in mammalian genomes.4 Rather than mere genomic “junk”, retronuons5,6 are often The process of retroposition (reverse transcrip- recruited or exapted into novel functions as they are tion of RNA into cDNA and concomitant genomic mobile carriers of potential control sequences integration)1–3 has contributed as much as 90% of (sometimes after a few minor alterations) and, thus, can equip existing genes with novel regulat- ory elements.5–15 Retronuons also provide existing 14,16,17 Present addresses: A. Ludwig, Department of genes with novel protein-coding domains, Biochemistry, University of Zu¨ rich, Winterthurerstrasse and even generate novel genes,5,18,19 including 190, CH-8057 Zu¨ rich, Switzerland; V. Yu. Kuryshev, those encoding non-messenger RNAs.20,21 Molecular Genome Analysis, German Cancer Research Themostabundantclassofretronuonsin Center, Im Neuenheimer Feld 580, D-69120 Heidelberg, vertebrate genomes are the short interspersed Germany. elements (SINEs).22 Most SINEs originated by Abbreviations used: SINE, short interspersed element; retroposition of tRNAs,23 tRNA-related RNAs or SRP, signal recognition particle; snoRNA, small nucleolar signal recognition particle (SRP) RNA (7SL RNA; fl, full-length; sc, small cytoplasmic; DSE, distal 24–27 sequence element; FLAM, free left Alu monomer; PSE, RNA). The SRP RNA-related Alu elements proximal sequence element. constitute the major SINE family in primates and 28,29 E-mail address of the corresponding author: exist in both monomeric and dimeric form. [email protected] Only a limited number of active Alu source (master) 0022-2836/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. Neural Dimeric Alu RNA in a Prosimian Branch 201 genes have given rise to the O106 Alu copies in other Lemuriformes (including Daubentonia primate genomes by successive waves of retro- madagascariensis), three other Lorisiformes, one positional activity.26,27,30 In certain lineages and at additional tarsier species as well as the colugo, a certain times, multiple source genes can be active in non-primate, but presumably primate-related parallel, as shown for the BC1 RNA-related retro- mammal (Cynocephalus variegatus, Dermoptera).55 nuons (ID elements) in rodents8,9 and Alu elements in primates.8,9,31 Apart from selective constraint on the source RNA, the redundancy of active elements Results might contribute to survival of retronuons in genomes. Despite the huge number of Alu element The G. moholi G22 Alu element is transcribed in copies in primate genomes, only a few Alu the brain transcripts have been observed in vivo.28,32–34 Clearly, 50 flanking sequences are important for The BC200 RNA gene is conserved and tran- autonomous transcription of SINEs.21,34–39 There- scribed in the anthropoid brain,43 but is absent from fore, the genomic environment, which is unique for orthologous loci of G. moholi, E. coronatus and each individual SINE, plays a decisive role in T. syrichta.44 While the strepsirrhine (G. moholi and whether a SINE is transcriptionally active or E. coronatus) loci harbour a dimeric Alu element at silent.6,8,40 exactly the same chromosomal location, the BC200 RNA, a neuronal, small non-messenger T. syrichta locus is devoid of any repetitive element. RNA, originated from a free left Alu monomer Unlike the E. coronatus Alu L13, the G. moholi Alu (FLAM)-C-like monomeric Alu element.21,41 The G22 preserved its internal box A and B promoter BC200 RNA gene represents one of the rare elements and its CpG doublets. Thus, we first members of this repetitive DNA family that is examined whether the G22 Alu would be tran- transcriptionally and retropositionally active.42–44 scriptionally active in the G. moholi brain, akin to Like its possible functional analogue in rodents, BC200 RNA in anthropoids. BC1 RNA,20 BC200 RNA is transcribed in neurons45 We performed Northern hybridization of total predominantly by RNA polymerase III21 and RNA isolated from various tissues of G. moholi, transported to dendrites as a ribonucleoprotein E. coronatus, T. syrichta and human, and probed for particle.46–49 the G22 and L13 Alu elements using several The gene encoding BC200 RNA has been mapped complementary oligonucleotides (Figure 1). An to chromosome 2p16,50 but the human genome oligonucleotide specific for the lorisiform G22 Alu sequence places it to band 2p21 between the element (G22_30) detected a single band in the CALM2 (calmodulin 2) and the TACSTD1 galago brain exhibiting an apparent size of w340 nt (tumour-associated calcium signal transducer 1) (Figure 1(a)). A “generic” probe complementary to genes.51 The gene is conserved in all anthropoids the Alu 50 domain (Alu_50) recognized, in addition including Old World monkeys, New World to the G22 Alu RNA, a transcript with an apparent monkeys and hominoids.43 V. Yu. K. et al. showed size of 300 nt. This transcript was detected in that the BC200 RNA gene is absent from ortho- E. coronatus and G. moholi tissues, but not in logous loci in representatives of the strepsirrhines T. syrichta and human samples (Figure 1(b)). The (Lorisiformes and Lemuriformes) and tarsiers, lack of any signal in tarsier and human tissues suggesting that the gene has arisen on the lineage reduces the possibility of cross-hybridization to 7SL leading to anthropoids after the separation of RNA (see Figure 3) and rather suggests that there is Strepsirrhini and Haplorrhini (tarsiers and anthro- an additional distinct Alu retronuon expressed in poids; for phylogenetic affiliations see Schmitz the G. moholi and E. coronatus tissues examined. et al.52).44 Surprisingly, the G. moholi (lorisiform) In order to probe for the E. coronatus L13 Alu and E. coronatus (lemuriform) loci harbor a dimeric element, we used two distinct oligonucleotides Alu element at the orthologous position. This sets (L13_insert and L13_30). Both oligonucleotides apart the aforementioned strepsirrhines from failed to detect a transcript in E. coronatus tissues tarsiers, whose orthologous loci are devoid of any that might correspond to the L13 Alu (data not repetitive element.44 Interestingly, the G. moholi Alu shown). Unexpectedly, however, the oligonucleo- (referred to as G22) features 21 preserved CpG tide probe L13_insert detected a band with an doublets (usually the first to change in genomic apparent size of 210 nt in human brain and, to a sequences released from purifying selection),53,54 lesser degree, in G. moholi brain and liver whereas the E. coronatus Alu (referred to as L13) (Figure 1(c)). This points to yet another distinct features only 11 CpG doublets. The conservation of transcript that is not necessarily Alu-related. With CpG doublets is an indication for transcriptional respect to the G. moholi G22 Alu element, our data activity and functionality, as had been shown for the indicate that it is prevalently, perhaps exclusively, BC200 RNA gene.41,43 This prompted us to examine transcribed in the brain, while the E. coronatus Alu whether G22 is transcribed in the G. moholi brain, L13 is transcriptionally silent. This observation akin to BC200 RNA in anthropoids. In order to prompted us to examine whether other lorisiform examine the strepsirrhine locus corresponding to and lemuriform species also harbour a dimeric the BC200 RNA gene locus in more detail, we Alu element at that chromosomal position. Thus, PCR-amplified and sequenced the locus of five we PCR-amplified, sequenced and analysed 202 Neural Dimeric Alu RNA in a Prosimian Branch as well as the outgroup sequences of colugo and mouse (Figure 2). As the sequences of the dimeric Alu elements in the two strepsirrhine lineages are quite divergent, we asked whether the lorisiform G22 and lemuri- form L13 Alu elements descend from a common Alu element or from independent progenitors. To this end, we aligned and compared the G22 and L13 Alu elements with the human AluJo consensus sequence, which is believed to be one of the most ancient dimeric Alu elements,29 and thus the closest relative of the strepsirrhine Alu elements examined here,44 as well as with lorisiform and lemuriform Alu consensus sequences (GS1, Gal and Lem-S; Figure 3).
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