The landscape of C. elegans 3′UTRs

Marco Mangone; Arun Prasad Manoharan; Danielle Thierry-Mieg; Jean Thierry-Mieg; Ting Han; Sebastian D. Mackowiak; Emily Mis; Charles Zegar; Michelle R. Gutwein; Vishal Khivansara; Oliver Attie; Kevin Chen; Kourosh Salehi-Ashtiani; Marc Vidal; Timothy T. Harkins; Pascal Bouffard; Yutaka Suzuki; Sumio Sugano; Yuji Kohara; Nikolaus Rajewsky; Fabio Piano; Kristin C. Gunsalus; John K. Kim

doi:10.1126/science.1191244

The landscape of C. elegans 3′UTRs

Marco Mangone, Arun Prasad Manoharan, Danielle Thierry-Mieg, Jean Thierry-Mieg, Ting Han, Sebastian D. Mackowiak, Emily Mis, Charles Zegar, Michelle R. Gutwein, Vishal Khivansara, Oliver Attie, Kevin Chen, Kourosh Salehi-Ashtiani, Marc Vidal, Timothy T. Harkins, Pascal Bouffard, Yutaka Suzuki, Sumio Sugano, Yuji Kohara, Nikolaus RajewskyFabio Piano, Kristin C. Gunsalus, John K. Kim

Research output: Contribution to journal › Article › peer-review

210 Scopus citations

Abstract

Three-prime untranslated regions (3′UTRs) of metazoan messenger RNAs (mRNAs) contain numerous regulatory elements, yet remain largely uncharacterized. Using polyA capture, 3′ rapid amplification of complementary DNA (cDNA) ends, full-length cDNAs, and RNA-seq, we defined ~26,000 distinct 3′UTRs in Caenorhabditis elegans for ∼85% of the 18,328 experimentally supported protein-coding genes and revised ∼40% of gene models. Alternative 3′UTR isoforms are frequent, often differentially expressed during development. Average 3′UTR length decreases with animal age. Surprisingly, no polyadenylation signal (PAS) was detected for 13% of polyadenylation sites, predominantly among shorter alternative isoforms. Trans-spliced (versus non-trans-spliced) mRNAs possess longer 3′UTRs and frequently contain no PAS or variant PAS. We identified conserved 3?UTR motifs, isoform-specific predicted microRNA target sites, and polyadenylation of most histone genes. Our data reveal a rich complexity of 3′UTRs, both genome-wide and throughout development.

Original language	English (US)
Pages (from-to)	432-435
Number of pages	4
Journal	Science
Volume	329
Issue number	5990
DOIs	https://doi.org/10.1126/science.1191244
State	Published - Jul 23 2010
Externally published	Yes

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Mangone, M., Manoharan, A. P., Thierry-Mieg, D., Thierry-Mieg, J., Han, T., Mackowiak, S. D., Mis, E., Zegar, C., Gutwein, M. R., Khivansara, V., Attie, O., Chen, K., Salehi-Ashtiani, K., Vidal, M., Harkins, T. T., Bouffard, P., Suzuki, Y., Sugano, S., Kohara, Y., ... Kim, J. K. (2010). The landscape of C. elegans 3′UTRs. Science, 329(5990), 432-435. https://doi.org/10.1126/science.1191244

Mangone, M, Manoharan, AP, Thierry-Mieg, D, Thierry-Mieg, J, Han, T, Mackowiak, SD, Mis, E, Zegar, C, Gutwein, MR, Khivansara, V, Attie, O, Chen, K, Salehi-Ashtiani, K, Vidal, M, Harkins, TT, Bouffard, P, Suzuki, Y, Sugano, S, Kohara, Y, Rajewsky, N, Piano, F, Gunsalus, KC & Kim, JK 2010, 'The landscape of C. elegans 3′UTRs', Science, vol. 329, no. 5990, pp. 432-435. https://doi.org/10.1126/science.1191244

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title = "The landscape of C. elegans 3′UTRs",

abstract = "Three-prime untranslated regions (3′UTRs) of metazoan messenger RNAs (mRNAs) contain numerous regulatory elements, yet remain largely uncharacterized. Using polyA capture, 3′ rapid amplification of complementary DNA (cDNA) ends, full-length cDNAs, and RNA-seq, we defined ~26,000 distinct 3′UTRs in Caenorhabditis elegans for ∼85% of the 18,328 experimentally supported protein-coding genes and revised ∼40% of gene models. Alternative 3′UTR isoforms are frequent, often differentially expressed during development. Average 3′UTR length decreases with animal age. Surprisingly, no polyadenylation signal (PAS) was detected for 13% of polyadenylation sites, predominantly among shorter alternative isoforms. Trans-spliced (versus non-trans-spliced) mRNAs possess longer 3′UTRs and frequently contain no PAS or variant PAS. We identified conserved 3?UTR motifs, isoform-specific predicted microRNA target sites, and polyadenylation of most histone genes. Our data reveal a rich complexity of 3′UTRs, both genome-wide and throughout development.",

author = "Marco Mangone and Manoharan, {Arun Prasad} and Danielle Thierry-Mieg and Jean Thierry-Mieg and Ting Han and Mackowiak, {Sebastian D.} and Emily Mis and Charles Zegar and Gutwein, {Michelle R.} and Vishal Khivansara and Oliver Attie and Kevin Chen and Kourosh Salehi-Ashtiani and Marc Vidal and Harkins, {Timothy T.} and Pascal Bouffard and Yutaka Suzuki and Sumio Sugano and Yuji Kohara and Nikolaus Rajewsky and Fabio Piano and Gunsalus, {Kristin C.} and Kim, {John K.}",

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AU - Kohara, Yuji

AU - Rajewsky, Nikolaus

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AU - Kim, John K.

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N2 - Three-prime untranslated regions (3′UTRs) of metazoan messenger RNAs (mRNAs) contain numerous regulatory elements, yet remain largely uncharacterized. Using polyA capture, 3′ rapid amplification of complementary DNA (cDNA) ends, full-length cDNAs, and RNA-seq, we defined ~26,000 distinct 3′UTRs in Caenorhabditis elegans for ∼85% of the 18,328 experimentally supported protein-coding genes and revised ∼40% of gene models. Alternative 3′UTR isoforms are frequent, often differentially expressed during development. Average 3′UTR length decreases with animal age. Surprisingly, no polyadenylation signal (PAS) was detected for 13% of polyadenylation sites, predominantly among shorter alternative isoforms. Trans-spliced (versus non-trans-spliced) mRNAs possess longer 3′UTRs and frequently contain no PAS or variant PAS. We identified conserved 3?UTR motifs, isoform-specific predicted microRNA target sites, and polyadenylation of most histone genes. Our data reveal a rich complexity of 3′UTRs, both genome-wide and throughout development.

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The landscape of C. elegans 3′UTRs

Abstract

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