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Article ; Online: Reply by Authors.

Han, Daniel S / Walker, Jonathan P / Nicklawsky, Andrew / Boxley, Peter / Halstead, N Valeska / Tonzi, Michael / Hecht, Sarah L / Staley, Alyse / Eguchi, Megan / Cockburn, Myles G / Roach, Jonathan P / Saltzman, Amanda F / Cost, Nicholas G

The Journal of urology

2023 Volume 209, Issue 3, Page(s) 590

Language	English
Publishing date	2023-03-01
Publishing country	United States
Document type	Journal Article ; Comment
ZDB-ID	3176-8
ISSN	1527-3792 ; 0022-5347
ISSN (online)	1527-3792
ISSN	0022-5347
DOI	10.1097/JU.0000000000003092.02
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Article: Global impact of aberrant splicing on human gene expression levels.

Fair, Benjamin / Najar, Carlos Buen Abad / Zhao, Junxing / Lozano, Stephanie / Reilly, Austin / Mossian, Gabriela / Staley, Jonathan P / Wang, Jingxin / Li, Yang I

bioRxiv : the preprint server for biology

2023

Abstract: Alternative splicing (AS) is pervasive in human genes, yet the specific function of most AS events remains unknown. It is widely assumed that the primary function of AS is to diversify the proteome, however AS can also influence gene expression levels by ...

Abstract	Alternative splicing (AS) is pervasive in human genes, yet the specific function of most AS events remains unknown. It is widely assumed that the primary function of AS is to diversify the proteome, however AS can also influence gene expression levels by producing transcripts rapidly degraded by nonsense-mediated decay (NMD). Currently, there are no precise estimates for how often the coupling of AS and NMD (AS-NMD) impacts gene expression levels because rapidly degraded NMD transcripts are challenging to capture. To better understand the impact of AS on gene expression levels, we analyzed population-scale genomic data in lymphoblastoid cell lines across eight molecular assays that capture gene regulation before, during, and after transcription and cytoplasmic decay. Sequencing nascent mRNA transcripts revealed frequent aberrant splicing of human introns, which results in remarkably high levels of mRNA transcripts subject to NMD. We estimate that ~15% of all protein-coding transcripts are degraded by NMD, and this estimate increases to nearly half of all transcripts for lowly-expressed genes with many introns. Leveraging genetic variation across cell lines, we find that GWAS trait-associated loci explained by AS are similarly likely to associate with NMD-induced expression level differences as with differences in protein isoform usage. Additionally, we used the splice-switching drug risdiplam to perturb AS at hundreds of genes, finding that ~3/4 of the splicing perturbations induce NMD. Thus, we conclude that AS-NMD substantially impacts the expression levels of most human genes. Our work further suggests that much of the molecular impact of AS is mediated by changes in protein expression levels rather than diversification of the proteome.
Language	English
Publishing date	2023-10-16
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.13.557588
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Article ; Online: Termination of pre-mRNA splicing requires that the ATPase and RNA unwindase Prp43p acts on the catalytic snRNA U6.

Toroney, Rebecca / Nielsen, Klaus H / Staley, Jonathan P

Genes & development

2019 Volume 33, Issue 21-22, Page(s) 1555–1574

Abstract: The termination of pre-mRNA splicing functions to discard suboptimal substrates, thereby enhancing fidelity, and to release excised introns in a manner coupled to spliceosome disassembly, thereby allowing recycling. The mechanism of termination, ... ...

Abstract	The termination of pre-mRNA splicing functions to discard suboptimal substrates, thereby enhancing fidelity, and to release excised introns in a manner coupled to spliceosome disassembly, thereby allowing recycling. The mechanism of termination, including the RNA target of the DEAH-box ATPase Prp43p, remains ambiguous. We discovered a critical role for nucleotides at the 3' end of the catalytic U6 small nuclear RNA in splicing termination. Although conserved sequence at the 3' end is not required, 2' hydroxyls are, paralleling requirements for Prp43p biochemical activities. Although the 3' end of U6 is not required for recruiting Prp43p to the spliceosome, the 3' end cross-links directly to Prp43p in an RNA-dependent manner. Our data indicate a mechanism of splicing termination in which Prp43p translocates along U6 from the 3' end to disassemble the spliceosome and thereby release suboptimal substrates or excised introns. This mechanism reveals that the spliceosome becomes primed for termination at the same stage it becomes activated for catalysis, implying a requirement for stringent control of spliceosome activity within the cell.
MeSH term(s)	Adenosine Triphosphatases/metabolism ; DEAD-box RNA Helicases/metabolism ; Introns/genetics ; Protein Binding ; RNA Splicing/genetics ; RNA Splicing/physiology ; RNA, Small Nuclear/metabolism ; Saccharomyces cerevisiae Proteins/metabolism ; Spliceosomes/metabolism
Chemical Substances	RNA, Small Nuclear ; Saccharomyces cerevisiae Proteins ; U6 small nuclear RNA ; Adenosine Triphosphatases (EC 3.6.1.-) ; PRP43 protein, S cerevisiae (EC 3.6.1.-) ; DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2019-09-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	806684-x
ISSN	1549-5477 ; 0890-9369
ISSN (online)	1549-5477
ISSN	0890-9369
DOI	10.1101/gad.328294.119
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Article ; Online: Reverse transcriptases lend a hand in splicing catalysis.

Piccirilli, Joseph A / Staley, Jonathan P

Nature structural & molecular biology

2016 Volume 23, Issue 6, Page(s) 507–509

MeSH term(s)	Clostridiales/enzymology ; Cryoelectron Microscopy ; Crystallography, X-Ray ; DNA/metabolism ; Endoribonucleases/chemistry ; Endoribonucleases/metabolism ; Endoribonucleases/ultrastructure ; Lactococcus lactis/enzymology ; Models, Molecular ; Nucleotidyltransferases/chemistry ; Nucleotidyltransferases/metabolism ; Nucleotidyltransferases/ultrastructure ; Protein Conformation ; RNA Splicing ; RNA-Directed DNA Polymerase/chemistry ; RNA-Directed DNA Polymerase/metabolism ; RNA-Directed DNA Polymerase/ultrastructure ; Recombination, Genetic
Chemical Substances	DNA (9007-49-2) ; Nucleotidyltransferases (EC 2.7.7.-) ; mRNA maturase (EC 2.7.7.-) ; RNA-Directed DNA Polymerase (EC 2.7.7.49) ; Endoribonucleases (EC 3.1.-)
Language	English
Publishing date	2016-06-06
Publishing country	United States
Document type	Journal Article
ZDB-ID	2126708-X
ISSN	1545-9985 ; 1545-9993
ISSN (online)	1545-9985
ISSN	1545-9993
DOI	10.1038/nsmb.3242
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Article ; Online: Pediatric Small Renal Masses: Can Tumor Size Predict Histology and the Potential for Nephron-sparing Surgery?

The Journal of urology

2022 Volume 209, Issue 3, Page(s) 582–590

Abstract: Purpose: The majority of children with unilateral renal masses suspicious for malignancy undergo radical nephrectomy, while nephron-sparing surgery is reserved for select cases. We investigated the impact of tumor size on the probability of histology. ... ...

Abstract	Purpose: The majority of children with unilateral renal masses suspicious for malignancy undergo radical nephrectomy, while nephron-sparing surgery is reserved for select cases. We investigated the impact of tumor size on the probability of histology. We hypothesized that pediatric small renal masses are more likely benign or non-Wilms tumor, thus potentially appropriate for nephron-sparing surgery. Materials and methods: The SEER (Surveillance, Epidemiology, and End Results) database was analyzed for patients aged 0-18 years diagnosed with a unilateral renal mass from 2000-2016. Statistical analysis was performed to help determine a tumor size cut point to predict Wilms tumor and assess the predictive value of tumor size on Wilms tumor histology. Additionally, a retrospective review was performed of patients 0-18 years old who underwent surgery for a unilateral renal mass at a single institution from 2005-2019. Statistical analysis was performed to assess the predictive value of tumor size on final histology. Results: From the SEER analysis, 2,016 patients were included. A total of 1,672 tumors (82.9%) were Wilms tumor. Analysis revealed 4 cm to be a suitable cut point to distinguish non-Wilms tumor. Tumors ≥4 cm were more likely Wilms tumor (OR 2.67, Conclusions: The probability that a pediatric unilateral renal mass is Wilms tumor increases with tumor size. Four centimeters is a logical cut point to start the conversation around defining pediatric small renal masses and may help predict nephron-sparing surgery-appropriate histology.
MeSH term(s)	Child ; Humans ; Infant, Newborn ; Infant ; Child, Preschool ; Adolescent ; Kidney Neoplasms/surgery ; Kidney Neoplasms/pathology ; Nephrons/surgery ; Nephrons/pathology ; Wilms Tumor/surgery ; Nephrectomy/methods ; Retrospective Studies
Language	English
Publishing date	2022-11-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3176-8
ISSN	1527-3792 ; 0022-5347
ISSN (online)	1527-3792
ISSN	0022-5347
DOI	10.1097/JU.0000000000003092
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Article: The debranching enzyme Dbr1 regulates lariat turnover and intron splicing.

Buerer, Luke / Clark, Nathaniel E / Welch, Anastasia / Duan, Chaorui / Taggart, Allison J / Townley, Brittany A / Wang, Jing / Soemedi, Rachel / Rong, Stephen / Lin, Chien-Ling / Zeng, Yi / Katolik, Adam / Staley, Jonathan P / Damha, Masad J / Mosammaparast, Nima / Fairbrother, William G

Research square

2023

Abstract: The majority of genic transcription is intronic. Introns are removed by splicing as branched lariat RNAs which require rapid recycling. The branch site is recognized during splicing catalysis and later debranched by Dbr1 in the rate-limiting step of ... ...

Abstract	The majority of genic transcription is intronic. Introns are removed by splicing as branched lariat RNAs which require rapid recycling. The branch site is recognized during splicing catalysis and later debranched by Dbr1 in the rate-limiting step of lariat turnover. Through generation of the first viable
Language	English
Publishing date	2023-06-13
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-2931976/v1
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Article ; Online: The DExD/H-box ATPase Prp2p destabilizes and proofreads the catalytic RNA core of the spliceosome.

Wlodaver, Alissa M / Staley, Jonathan P

RNA (New York, N.Y.)

2014 Volume 20, Issue 3, Page(s) 282–294

Abstract: After undergoing massive RNA and protein rearrangements during assembly, the spliceosome undergoes a final, more subtle, ATP-dependent rearrangement that is essential for catalysis. This rearrangement requires the DEAH-box protein Prp2p, an RNA-dependent ...

Abstract	After undergoing massive RNA and protein rearrangements during assembly, the spliceosome undergoes a final, more subtle, ATP-dependent rearrangement that is essential for catalysis. This rearrangement requires the DEAH-box protein Prp2p, an RNA-dependent ATPase. Prp2p has been implicated in destabilizing interactions between the spliceosome and the protein complexes SF3 and RES, but a role for Prp2p in destabilizing RNA-RNA interactions has not been explored. Using directed molecular genetics in budding yeast, we have found that a cold-sensitive prp2 mutation is suppressed not only by mutations in SF3 and RES components but also by a range of mutations that disrupt the spliceosomal catalytic core element U2/U6 helix I, which is implicated in juxtaposing the 5' splice site and branch site and in positioning metal ions for catalysis within the context of a putative catalytic triplex; indeed, mutations in this putative catalytic triplex also suppressed a prp2 mutation. Remarkably, we also found that prp2 mutations rescue lethal mutations in U2/U6 helix I. These data provide evidence that RNA elements that comprise the catalytic core are already formed at the Prp2p stage and that Prp2p destabilizes these elements, directly or indirectly, both to proofread spliceosome activation and to promote reconfiguration of the spliceosome to a fully competent, catalytic conformation.
MeSH term(s)	Catalytic Domain ; DEAD-box RNA Helicases/chemistry ; DEAD-box RNA Helicases/genetics ; DEAD-box RNA Helicases/metabolism ; Mutation/genetics ; Nucleic Acid Conformation ; RNA Helicases/genetics ; RNA Helicases/metabolism ; RNA Splicing/genetics ; RNA, Catalytic/chemistry ; RNA, Catalytic/genetics ; RNA, Small Nuclear/genetics ; RNA, Small Nuclear/metabolism ; Saccharomyces cerevisiae/genetics ; Saccharomyces cerevisiae/growth & development ; Saccharomyces cerevisiae/metabolism ; Saccharomyces cerevisiae Proteins/chemistry ; Saccharomyces cerevisiae Proteins/genetics ; Saccharomyces cerevisiae Proteins/metabolism ; Spliceosomes/genetics
Chemical Substances	RNA, Catalytic ; RNA, Small Nuclear ; Saccharomyces cerevisiae Proteins ; U2 small nuclear RNA ; U6 small nuclear RNA ; PRP2 protein, S cerevisiae (EC 3.6.1.-) ; DEAD-box RNA Helicases (EC 3.6.4.13) ; RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2014-01-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1241540-6
ISSN	1469-9001 ; 1355-8382
ISSN (online)	1469-9001
ISSN	1355-8382
DOI	10.1261/rna.042598.113
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Article ; Online: Preoperative CA 19-9 Predicts Disease Progression in Colorectal Peritoneal Metastases Treated with Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy: An Analysis from the US HIPEC Collaborative.

Annals of surgical oncology

2024 Volume 31, Issue 5, Page(s) 3314–3324

Abstract: ... associated with dismal PFS at 2 years (8.9% elevated vs. 30% not elevated, p < 0.01). In 113 patients ... hazard ratio [HR] 2.88, p = 0.048). In the subgroup of patients who had received neoadjuvant therapy (NAT ...

Abstract	Introduction: Patients with colorectal peritoneal metastases (CRPM) are increasingly treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (CRS/HIPEC). Unfortunately, data identifying preoperative risk factors for poor oncologic outcomes after this procedure are limited. We aimed to determine the prognostic value of preoperative CEA, CA 125, and CA 19-9 on disease progression after CRS/HIPEC. Methods: Patients with CRPM treated with curative intent CRS/HIPEC from 12 participating sites in the United States from 2000 to 2017 were identified. Progression-free survival (PFS), defined as disease progression or recurrence, was the primary outcome. Results: In 279 patients who met inclusion criteria, the rate of disease progression was 63.8%, with a median PFS of 11 months (interquartile range [IQR] 5-20). Elevated CA 19-9 was associated with dismal PFS at 2 years (8.9% elevated vs. 30% not elevated, p < 0.01). In 113 patients who underwent upfront CRS/HIPEC, CA 19-9 emerged as the sole tumor marker independently predictive of worse PFS (hazard ratio [HR] 2.88, p = 0.048). In the subgroup of patients who had received neoadjuvant therapy (NAT), no variable was independently predictive of PFS. CA 19-9 levels over 37 U/ml were highly specific for accelerated disease progression after CRS/HIPEC. Lastly, there was no association between PFS and elevated CEA or CA 125. Conclusions: Elevated CA 19-9 is associated with decreased PFS in patients with CRPM. While traditionally CEA is the main tumor marker assessed in colon cancer, we found that CA 19-9 may better inform preoperative risk stratification for poor oncologic outcomes in patients with CRPM. However, prospective studies are required to confirm this association.
MeSH term(s)	Humans ; Hyperthermic Intraperitoneal Chemotherapy ; Peritoneal Neoplasms/secondary ; Colorectal Neoplasms/pathology ; Cytoreduction Surgical Procedures ; Hyperthermia, Induced ; Chemotherapy, Cancer, Regional Perfusion ; Disease Progression ; Biomarkers, Tumor ; Combined Modality Therapy ; Survival Rate ; Antineoplastic Combined Chemotherapy Protocols/therapeutic use ; Retrospective Studies
Chemical Substances	Biomarkers, Tumor
Language	English
Publishing date	2024-02-03
Publishing country	United States
Document type	Journal Article
ZDB-ID	1200469-8
ISSN	1534-4681 ; 1068-9265
ISSN (online)	1534-4681
ISSN	1068-9265
DOI	10.1245/s10434-024-14890-0
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Article ; Online: Splicing fidelity: DEAD/H-box ATPases as molecular clocks.

Koodathingal, Prakash / Staley, Jonathan P

RNA biology

2013 Volume 10, Issue 7, Page(s) 1073–1079

Abstract: The spliceosome discriminates against suboptimal substrates, both during assembly and catalysis, thereby enhancing specificity during pre-mRNA splicing. Central to such fidelity mechanisms are a conserved subset of the DEAD- and DEAH-box ATPases, which ... ...

Abstract	The spliceosome discriminates against suboptimal substrates, both during assembly and catalysis, thereby enhancing specificity during pre-mRNA splicing. Central to such fidelity mechanisms are a conserved subset of the DEAD- and DEAH-box ATPases, which belong to a superfamily of proteins that mediate RNP rearrangements in almost all RNA-dependent processes in the cell. Through an investigation of the mechanisms contributing to the specificity of 5' splice site cleavage, two related reports, one from our lab and the other from the Cheng lab, have provided insights into fidelity mechanisms utilized by the spliceosome. In our work, we found evidence for a kinetic proofreading mechanism in splicing in which the DEAH-box ATPase Prp16 discriminates against substrates undergoing slow 5' splice site cleavage. Additionally, our study revealed that discriminated substrates are discarded through a general spliceosome disassembly pathway, mediated by another DEAH-box ATPase Prp43. In their work, Tseng et al. described the underlying molecular events through which Prp16 discriminates against a splicing substrate during 5' splice site cleavage. Here, we present a synthesis of these two studies and, additionally, provide the first biochemical evidence for discrimination of a suboptimal splicing substrate just prior to 5' splice site cleavage. Together, these findings support a general mechanism for a ubiquitous superfamily of ATPases in enhancing specificity during RNA-dependent processes in the cell.
MeSH term(s)	DEAD-box RNA Helicases/metabolism ; Introns ; RNA Precursors/genetics ; RNA Precursors/metabolism ; RNA Splice Sites ; RNA Splicing/physiology ; Spliceosomes/metabolism ; Substrate Specificity
Chemical Substances	RNA Precursors ; RNA Splice Sites ; DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2013-06-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2159587-2
ISSN	1555-8584 ; 1555-8584
ISSN (online)	1555-8584
ISSN	1555-8584
DOI	10.4161/rna.25245
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Article ; Online: Profiling lariat intermediates reveals genetic determinants of early and late co-transcriptional splicing.

Zeng, Yi / Fair, Benjamin J / Zeng, Huilin / Krishnamohan, Aiswarya / Hou, Yichen / Hall, Johnathon M / Ruthenburg, Alexander J / Li, Yang I / Staley, Jonathan P

Molecular cell

2022 Volume 82, Issue 24, Page(s) 4681–4699.e8

Abstract: Long introns with short exons in vertebrate genes are thought to require spliceosome assembly across exons (exon definition), rather than introns, thereby requiring transcription of an exon to splice an upstream intron. Here, we developed CoLa-seq (co- ... ...

Abstract	Long introns with short exons in vertebrate genes are thought to require spliceosome assembly across exons (exon definition), rather than introns, thereby requiring transcription of an exon to splice an upstream intron. Here, we developed CoLa-seq (co-transcriptional lariat sequencing) to investigate the timing and determinants of co-transcriptional splicing genome wide. Unexpectedly, 90% of all introns, including long introns, can splice before transcription of a downstream exon, indicating that exon definition is not obligatory for most human introns. Still, splicing timing varies dramatically across introns, and various genetic elements determine this variation. Strong U2AF2 binding to the polypyrimidine tract predicts early splicing, explaining exon definition-independent splicing. Together, our findings question the essentiality of exon definition and reveal features beyond intron and exon length that are determinative for splicing timing.
MeSH term(s)	Humans ; Base Sequence ; RNA Splicing ; Introns/genetics ; Exons/genetics ; Alternative Splicing
Language	English
Publishing date	2022-11-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2022.11.004
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