SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)

Abstract Background Messenger RNA 3’ untranslated regions (3’UTRs) control many aspects of gene expression and determine where the transcript will terminate. The polyadenylation signal (PAS) AAUAAA (AATAAA in DNA) is a key regulator of transcript termination and this hexamer, or a similar sequence,...

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Main Authors: Jessica D. Choi, Lelani A. Del Pinto, Nathan B. Sutter
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Mobile DNA
Online Access:https://doi.org/10.1186/s13100-024-00338-5
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author Jessica D. Choi
Lelani A. Del Pinto
Nathan B. Sutter
author_facet Jessica D. Choi
Lelani A. Del Pinto
Nathan B. Sutter
author_sort Jessica D. Choi
collection DOAJ
description Abstract Background Messenger RNA 3’ untranslated regions (3’UTRs) control many aspects of gene expression and determine where the transcript will terminate. The polyadenylation signal (PAS) AAUAAA (AATAAA in DNA) is a key regulator of transcript termination and this hexamer, or a similar sequence, is very frequently found within 30 bp of 3’UTR ends. Short interspersed element (SINE) retrotransposons are found throughout genomes in high copy numbers. When inserted into genes they can disrupt expression, alter splicing, or cause nuclear retention of mRNAs. The genomes of the domestic dog and other carnivores carry hundreds of thousands of Can-SINEs, a tRNA-related SINE with transcription termination potential. Because of this we asked whether Can-SINEs may terminate transcript in some dog genes. Results Each of the dog’s nine Can-SINE consensus sequences carry an average of three AATAAA PASs on their sense strands but zero on their antisense strands. Consistent with the idea that Can-SINEs can terminate transcripts, we find that sense-oriented Can-SINEs are approximately ten times more frequent at 3’ ends of 3’UTRs compared to further upstream within 3’UTRs. Furthermore, the count of AATAAA PASs on head-to-tail SINE sequences differs significantly between sense and antisense-oriented retrotransposons in transcripts. Can-SINEs near 3’UTR ends are likely to carry an AATAAA motif on the mRNA sense strand while those further upstream are not. We identified loci where Can-SINE insertion has truncated or altered a 3’UTR of the dog genome (dog 3’UTR) compared to the human ortholog. Dog 3’UTRs have peaks of AATAAA PAS frequency at 28, 32, and 36 bp from the end. The periodicity is partly explained by TAAA(n) repeats within Can-SINE AT-rich tails. We annotated all repeat-masked Can-SINE copies in the Boxer reference genome and found that the young SINEC_Cf type has a mode of 15 bp length for target site duplications (TSDs). All dog Can-SINE types favor integration at TSDs beginning with A(4). Conclusion Dog Can-SINE retrotransposition has imported AATAAA PASs into gene transcripts and led to alteration of 3’UTRs. AATAAA sequences are selectively removed from Can-SINEs in introns and upstream 3’UTR regions but are retained at the far downstream end of 3’UTRs, which we infer reflects their role as termination sequences for these transcripts.
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spelling doaj-art-a026d0e8ac0341be841aa47eb4cfc5202025-01-05T12:32:57ZengBMCMobile DNA1759-87532025-01-0116111210.1186/s13100-024-00338-5SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)Jessica D. Choi0Lelani A. Del Pinto1Nathan B. Sutter2Department of Biology, La Sierra UniversityDepartment of Biology, La Sierra UniversityDepartment of Biology, La Sierra UniversityAbstract Background Messenger RNA 3’ untranslated regions (3’UTRs) control many aspects of gene expression and determine where the transcript will terminate. The polyadenylation signal (PAS) AAUAAA (AATAAA in DNA) is a key regulator of transcript termination and this hexamer, or a similar sequence, is very frequently found within 30 bp of 3’UTR ends. Short interspersed element (SINE) retrotransposons are found throughout genomes in high copy numbers. When inserted into genes they can disrupt expression, alter splicing, or cause nuclear retention of mRNAs. The genomes of the domestic dog and other carnivores carry hundreds of thousands of Can-SINEs, a tRNA-related SINE with transcription termination potential. Because of this we asked whether Can-SINEs may terminate transcript in some dog genes. Results Each of the dog’s nine Can-SINE consensus sequences carry an average of three AATAAA PASs on their sense strands but zero on their antisense strands. Consistent with the idea that Can-SINEs can terminate transcripts, we find that sense-oriented Can-SINEs are approximately ten times more frequent at 3’ ends of 3’UTRs compared to further upstream within 3’UTRs. Furthermore, the count of AATAAA PASs on head-to-tail SINE sequences differs significantly between sense and antisense-oriented retrotransposons in transcripts. Can-SINEs near 3’UTR ends are likely to carry an AATAAA motif on the mRNA sense strand while those further upstream are not. We identified loci where Can-SINE insertion has truncated or altered a 3’UTR of the dog genome (dog 3’UTR) compared to the human ortholog. Dog 3’UTRs have peaks of AATAAA PAS frequency at 28, 32, and 36 bp from the end. The periodicity is partly explained by TAAA(n) repeats within Can-SINE AT-rich tails. We annotated all repeat-masked Can-SINE copies in the Boxer reference genome and found that the young SINEC_Cf type has a mode of 15 bp length for target site duplications (TSDs). All dog Can-SINE types favor integration at TSDs beginning with A(4). Conclusion Dog Can-SINE retrotransposition has imported AATAAA PASs into gene transcripts and led to alteration of 3’UTRs. AATAAA sequences are selectively removed from Can-SINEs in introns and upstream 3’UTR regions but are retained at the far downstream end of 3’UTRs, which we infer reflects their role as termination sequences for these transcripts.https://doi.org/10.1186/s13100-024-00338-5
spellingShingle Jessica D. Choi
Lelani A. Del Pinto
Nathan B. Sutter
SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)
Mobile DNA
title SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)
title_full SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)
title_fullStr SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)
title_full_unstemmed SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)
title_short SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)
title_sort sine retrotransposons import polyadenylation signals to 3 utrs in dog canis familiaris
url https://doi.org/10.1186/s13100-024-00338-5
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AT nathanbsutter sineretrotransposonsimportpolyadenylationsignalsto3utrsindogcanisfamiliaris