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Article ; Online: A Kuhnian revolution in molecular biology: Most genes in complex organisms express regulatory RNAs.

Mattick, John S

BioEssays : news and reviews in molecular, cellular and developmental biology

2023 Volume 45, Issue 9, Page(s) e2300080

Abstract: Thomas Kuhn described the progress of science as comprising occasional paradigm shifts separated by interludes of 'normal science'. The paradigm that has held sway since the inception of molecular biology is that genes (mainly) encode proteins. In ... ...

Abstract	Thomas Kuhn described the progress of science as comprising occasional paradigm shifts separated by interludes of 'normal science'. The paradigm that has held sway since the inception of molecular biology is that genes (mainly) encode proteins. In parallel, theoreticians posited that mutation is random, inferred that most of the genome in complex organisms is non-functional, and asserted that somatic information is not communicated to the germline. However, many anomalies appeared, particularly in plants and animals: the strange genetic phenomena of paramutation and transvection; introns; repetitive sequences; a complex epigenome; lack of scaling of (protein-coding) genes and increase in 'noncoding' sequences with developmental complexity; genetic loci termed 'enhancers' that control spatiotemporal gene expression patterns during development; and a plethora of 'intergenic', overlapping, antisense and intronic transcripts. These observations suggest that the original conception of genetic information was deficient and that most genes in complex organisms specify regulatory RNAs, some of which convey intergenerational information. Also see the video abstract here: https://youtu.be/qxeGwahBANw.
MeSH term(s)	RNA/genetics ; Introns/genetics ; Genome ; Gene Expression Regulation/genetics ; Molecular Biology
Chemical Substances	RNA (63231-63-0)
Language	English
Publishing date	2023-06-15
Publishing country	United States
Document type	Video-Audio Media ; Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	50140-2
ISSN	1521-1878 ; 0265-9247
ISSN (online)	1521-1878
ISSN	0265-9247
DOI	10.1002/bies.202300080
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Article: RNA out of the mist.

Mattick, John S

Trends in genetics : TIG

2022 Volume 39, Issue 3, Page(s) 187–207

Abstract: RNA has long been regarded primarily as the intermediate between genes and proteins. It was a surprise then to discover that eukaryotic genes are mosaics of mRNA sequences interrupted by large tracts of transcribed but untranslated sequences, and that ... ...

Abstract	RNA has long been regarded primarily as the intermediate between genes and proteins. It was a surprise then to discover that eukaryotic genes are mosaics of mRNA sequences interrupted by large tracts of transcribed but untranslated sequences, and that multicellular organisms also express many long 'intergenic' and antisense noncoding RNAs (lncRNAs). The identification of small RNAs that regulate mRNA translation and half-life did not disturb the prevailing view that animals and plant genomes are full of evolutionary debris and that their development is mainly supervised by transcription factors. Gathering evidence to the contrary involved addressing the low conservation, expression, and genetic visibility of lncRNAs, demonstrating their cell-specific roles in cell and developmental biology, and their association with chromatin-modifying complexes and phase-separated domains. The emerging picture is that most lncRNAs are the products of genetic loci termed 'enhancers', which marshal generic effector proteins to their sites of action to control cell fate decisions during development.
MeSH term(s)	Animals ; RNA, Long Noncoding/genetics ; Transcription Factors/genetics ; Chromatin ; RNA, Messenger ; Genome, Plant
Chemical Substances	RNA, Long Noncoding ; Transcription Factors ; Chromatin ; RNA, Messenger
Language	English
Publishing date	2022-12-15
Publishing country	England
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	619240-3
ISSN	1362-4555 ; 0168-9525 ; 0168-9479
ISSN (online)	1362-4555
ISSN	0168-9525 ; 0168-9479
DOI	10.1016/j.tig.2022.11.001
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Article ; Online: A Kuhnian revolution in molecular biology: Most genes in complex organisms express regulatory RNAs

Mattick, John S.

BioEssays. 2023 Sept., v. 45, no. 9 p.e2300080-

2023

Abstract: Thomas Kuhn described the progress of science as comprising occasional paradigm shifts separated by interludes of ‘normal science’. The paradigm that has held sway since the inception of molecular biology is that genes (mainly) encode proteins. In ... ...

Abstract	Thomas Kuhn described the progress of science as comprising occasional paradigm shifts separated by interludes of ‘normal science’. The paradigm that has held sway since the inception of molecular biology is that genes (mainly) encode proteins. In parallel, theoreticians posited that mutation is random, inferred that most of the genome in complex organisms is non‐functional, and asserted that somatic information is not communicated to the germline. However, many anomalies appeared, particularly in plants and animals: the strange genetic phenomena of paramutation and transvection; introns; repetitive sequences; a complex epigenome; lack of scaling of (protein‐coding) genes and increase in ‘noncoding’ sequences with developmental complexity; genetic loci termed ‘enhancers’ that control spatiotemporal gene expression patterns during development; and a plethora of ‘intergenic’, overlapping, antisense and intronic transcripts. These observations suggest that the original conception of genetic information was deficient and that most genes in complex organisms specify regulatory RNAs, some of which convey intergenerational information. Also see the video abstract here: https://youtu.be/qxeGwahBANw
Keywords	conception ; epigenome ; gene expression ; germ cells ; introns ; molecular biology ; mutation
Language	English
Dates of publication	2023-09
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	50140-2
ISSN	1521-1878 ; 0265-9247
ISSN (online)	1521-1878
ISSN	0265-9247
DOI	10.1002/bies.202300080
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Article ; Online: Natural antisense transcripts as versatile regulators of gene expression.

Werner, Andreas / Kanhere, Aditi / Wahlestedt, Claes / Mattick, John S

Nature reviews. Genetics

2024

Abstract: Long non-coding RNAs (lncRNAs) are emerging as a major class of gene products that have central roles in cell and developmental biology. Natural antisense transcripts (NATs) are an important subset of lncRNAs that are expressed from the opposite strand ... ...

Abstract	Long non-coding RNAs (lncRNAs) are emerging as a major class of gene products that have central roles in cell and developmental biology. Natural antisense transcripts (NATs) are an important subset of lncRNAs that are expressed from the opposite strand of protein-coding and non-coding genes and are a genome-wide phenomenon in both eukaryotes and prokaryotes. In eukaryotes, a myriad of NATs participate in regulatory pathways that affect expression of their cognate sense genes. Recent developments in the study of NATs and lncRNAs and large-scale sequencing and bioinformatics projects suggest that whether NATs regulate expression, splicing, stability or translation of the sense transcript is influenced by the pattern and degrees of overlap between the sense-antisense pair. Moreover, epigenetic gene regulatory mechanisms prevail in somatic cells whereas mechanisms dependent on the formation of double-stranded RNA intermediates are prevalent in germ cells. The modulating effects of NATs on sense transcript expression make NATs rational targets for therapeutic interventions.
Language	English
Publishing date	2024-04-17
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2035157-4
ISSN	1471-0064 ; 1471-0056
ISSN (online)	1471-0064
ISSN	1471-0056
DOI	10.1038/s41576-024-00723-z
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Article ; Online: RNA Regulatory Networks 2.0.

Enguita, Francisco J / Leitão, Ana Lúcia / Mattick, John S

International journal of molecular sciences

2023 Volume 24, Issue 10

Abstract: The central role of RNA molecules in cell biology has been an expanding subject of study since the proposal of the "RNA world" hypothesis 60 years ago [ ... ]. ...

Abstract	The central role of RNA molecules in cell biology has been an expanding subject of study since the proposal of the "RNA world" hypothesis 60 years ago [...].
MeSH term(s)	RNA/genetics ; Gene Regulatory Networks
Chemical Substances	RNA (63231-63-0)
Language	English
Publishing date	2023-05-19
Publishing country	Switzerland
Document type	Editorial
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms24109001
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Article ; Online: The State of Long Non-Coding RNA Biology.

Mattick, John S

Non-coding RNA

2018 Volume 4, Issue 3

Abstract: Transcriptomic studies have demonstrated that the vast majority of the genomes of mammals and other complex organisms is expressed in highly dynamic and cell-specific patterns to produce large numbers of intergenic, antisense and intronic long non- ... ...

Abstract	Transcriptomic studies have demonstrated that the vast majority of the genomes of mammals and other complex organisms is expressed in highly dynamic and cell-specific patterns to produce large numbers of intergenic, antisense and intronic long non-protein-coding RNAs (lncRNAs). Despite well characterized examples, their scaling with developmental complexity, and many demonstrations of their association with cellular processes, development and diseases, lncRNAs are still to be widely accepted as major players in gene regulation. This may reflect an underappreciation of the extent and precision of the epigenetic control of differentiation and development, where lncRNAs appear to have a central role, likely as organizational and guide molecules: most lncRNAs are nuclear-localized and chromatin-associated, with some involved in the formation of specialized subcellular domains. I suggest that a reassessment of the conceptual framework of genetic information and gene expression in the 4-dimensional ontogeny of spatially organized multicellular organisms is required. Together with this and further studies on their biology, the key challenges now are to determine the structure⁻function relationships of lncRNAs, which may be aided by emerging evidence of their modular structure, the role of RNA editing and modification in enabling epigenetic plasticity, and the role of RNA signaling in transgenerational inheritance of experience.
Language	English
Publishing date	2018-08-10
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2813993-8
ISSN	2311-553X ; 2311-553X
ISSN (online)	2311-553X
ISSN	2311-553X
DOI	10.3390/ncrna4030017
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Article ; Online: High frequency of intron retention and clustered H3K4me3-marked nucleosomes in short first introns of human long non-coding RNAs.

Dey, Pinki / Mattick, John S

Epigenetics & chromatin

2021 Volume 14, Issue 1, Page(s) 45

Abstract: Background: It is established that protein-coding exons are preferentially localized in nucleosomes. To examine whether the same is true for non-coding exons, we analysed nucleosome occupancy in and adjacent to internal exons in genes encoding long non- ... ...

Abstract	Background: It is established that protein-coding exons are preferentially localized in nucleosomes. To examine whether the same is true for non-coding exons, we analysed nucleosome occupancy in and adjacent to internal exons in genes encoding long non-coding RNAs (lncRNAs) in human CD4+ T cells and K562 cells. Results: We confirmed that internal exons in lncRNAs are preferentially associated with nucleosomes, but also observed an elevated signal from H3K4me3-marked nucleosomes in the sequences upstream of these exons. Examination of 200 genomic lncRNA loci chosen at random across all chromosomes showed that high-density regions of H3K4me3-marked nucleosomes, which we term 'slabs', are associated with genomic regions exhibiting intron retention. These retained introns occur in over 50% of lncRNAs examined and are mostly first introns with an average length of just 354 bp, compared to the average length of all human introns of 6355 and 7987 bp in mRNAs and lncRNAs, respectively. Removal of short introns from the dataset abrogated the high upstream H3K4me3 signal, confirming that the association of slabs and short lncRNA introns with intron retention holds genome-wide. The high upstream H3K4me3 signal is also associated with alternatively spliced exons, known to be prominent in lncRNAs. This phenomenon was not observed with mRNAs. Conclusions: There is widespread intron retention and clustered H3K4me3-marked nucleosomes in short first introns of human long non-coding RNAs, which raises intriguing questions about the relationship of IR to lncRNA function and chromatin organization.
MeSH term(s)	Histones/genetics ; Humans ; Introns ; Nucleosomes/genetics ; RNA, Long Noncoding/genetics
Chemical Substances	Histones ; Nucleosomes ; RNA, Long Noncoding ; histone H3 trimethyl Lys4
Language	English
Publishing date	2021-09-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2462129-8
ISSN	1756-8935 ; 1756-8935
ISSN (online)	1756-8935
ISSN	1756-8935
DOI	10.1186/s13072-021-00419-2
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Exploring the epitranscriptome by native RNA sequencing.

Begik, Oguzhan / Mattick, John S / Novoa, Eva Maria

RNA (New York, N.Y.)

2022 Volume 28, Issue 11, Page(s) 1430–1439

Abstract: Chemical RNA modifications, collectively referred to as the "epitranscriptome," are essential players in fine-tuning gene expression. Our ability to analyze RNA modifications has improved rapidly in recent years, largely due to the advent of high- ... ...

Abstract	Chemical RNA modifications, collectively referred to as the "epitranscriptome," are essential players in fine-tuning gene expression. Our ability to analyze RNA modifications has improved rapidly in recent years, largely due to the advent of high-throughput sequencing methodologies, which typically consist of coupling modification-specific reagents, such as antibodies or enzymes, to next-generation sequencing. Recently, it also became possible to map RNA modifications directly by sequencing native RNAs using nanopore technologies, which has been applied for the detection of a number of RNA modifications, such as N6-methyladenosine (m
MeSH term(s)	Sequence Analysis, RNA ; Pseudouridine/genetics ; Pseudouridine/metabolism ; RNA/genetics ; RNA/metabolism ; High-Throughput Nucleotide Sequencing ; RNA Processing, Post-Transcriptional ; Transcriptome
Chemical Substances	Pseudouridine (1445-07-4) ; RNA (63231-63-0)
Language	English
Publishing date	2022-09-14
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1241540-6
ISSN	1469-9001 ; 1355-8382
ISSN (online)	1469-9001
ISSN	1355-8382
DOI	10.1261/rna.079404.122
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Article ; Online: The potential of long noncoding RNA therapies.

Mercer, Tim R / Munro, Trent / Mattick, John S

Trends in pharmacological sciences

2022 Volume 43, Issue 4, Page(s) 269–280

Abstract: The human genome expresses vast numbers of long noncoding RNAs (lncRNA) that fulfil diverse roles in gene regulation, cell biology, development, and human disease. These roles are often mediated by sequence motifs and secondary structures bound by ... ...

Abstract	The human genome expresses vast numbers of long noncoding RNAs (lncRNA) that fulfil diverse roles in gene regulation, cell biology, development, and human disease. These roles are often mediated by sequence motifs and secondary structures bound by proteins and can regulate epigenetic, transcriptional, and translational pathways. These functional domains can be further optimised and engineered into RNA devices that are widely used in synthetic biology. We propose that natural lncRNA structures can be explored and exploited for the rational design and assembly of synthetic RNA therapies. This potential has been enabled by advances in the stability, immunogenicity, manufacture, and delivery of other RNA-based therapies, from which we can anticipate the pharmacological properties of lncRNA therapies that have not yet otherwise entered clinical trials.
MeSH term(s)	Gene Expression Regulation ; Genome, Human ; Humans ; RNA, Long Noncoding/genetics
Chemical Substances	RNA, Long Noncoding
Language	English
Publishing date	2022-02-10
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	282846-7
ISSN	1873-3735 ; 0165-6147
ISSN (online)	1873-3735
ISSN	0165-6147
DOI	10.1016/j.tips.2022.01.008
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Article: Probing the phenomics of noncoding RNA.

Mattick, John S

eLife

2013 Volume 2, Page(s) e01968

Abstract: Genetic knockout experiments on mice confirm that some long noncoding RNA molecules have developmental functions. ...

Abstract	Genetic knockout experiments on mice confirm that some long noncoding RNA molecules have developmental functions.
MeSH term(s)	Animals ; Brain/growth & development ; RNA, Long Noncoding/physiology
Chemical Substances	RNA, Long Noncoding
Language	English
Publishing date	2013-12-31
Publishing country	England
Document type	Journal Article ; Comment
ZDB-ID	2687154-3
ISSN	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.01968
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