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Wilson, M. D.

Publications and source records attributed to Wilson, M. D..

At least 19 recordsLinked to original sources

H2A.Z-H2B.V nucleosomes form a specialised scaffold for transcription initiation in Trypanosoma brucei

Regions of transcription initiation are often enriched in the histone variant H2A.Z. This is especially true in the divergent eukaryote Trypanosoma brucei, where broad domains of H2A.Z and a kinetoplastid-specific variant H2B.V define a limited number of polycistronic transcription start sites. To explore the chromatin underpinning this unusual transcription, we reconstituted H2A.Z-H2B.V nucleosomes in vitro and found that they are inherently unstable, form open chromatin structures, and serve as a direct interaction scaffold for gene regulators, in line with their role in transcription activation. A single particle cryo-EM structure reveals why H2A.Z-H2B.V form obligate dimers, pack differently within nucleosomes, and exhibit altered binding to DNA. We identified unique features of H2A.Z and H2B.V that result in differential activity of chromatin modifying enzymes, including the H2A.Z C-terminal tail and an atypical acidic patch. An affinity purification mass spectrometry screening approach revealed that H2A.Z-H2B.V nucleosomes have a distinct protein interaction profile, suggesting that interactions with chromatin factors are directly tuned for transcription control. Overall, this work reveals how trypanosome-specific histone features both inherently alter the biomechanical properties of nucleosomes as well as reshape chromatin binding and modification patterns at transcription start sites.

biochemistry↗

Unbiased Long-Read Whole-Genome Sequencing Enables High-Resolution Mapping of Transgene Concatenation and Off-target Genomic Disruption in a Mouse Model

Transgenic mouse models are indispensable for dissecting disease mechanisms; yet, their interpretability is frequently compromised by cryptic genomic alterations introduced during transgenesis. Thus, robust quality control strategies are needed to elucidate integration architecture and evaluate model performance when such unintended events occur. Here, we applied unbiased whole-genome long-read sequencing using the PacBio Revio to investigate a mouse model exhibiting unexpected transgene silencing, originally designed to recapitulate autosomal-dominant hereditary macular dystrophy driven by upregulation of a ZZEF1-ALOX15 fusion gene. Long-read sequencing analysis revealed a [≥]29-kb head-to-tail concatemer containing more than three copies of the transgene vector. Reconstruction of transgene-genome junctions revealed off-target integration of the concatemer into the calcium-sensing receptor gene (Casr), along with exogenous E. coli DNA, that together defined final transgene architecture. 5-methylcytosine profiling identified hypermethylation of the transgene promoter and additional phenotyping indicated disruption of endogenous Casr function resulting from the rearrangement. Our workflow enabled direct detection of transgene concatenation and off-target mapping. These findings establish long-read sequencing as a powerful and scalable quality control standard for genetically engineered animal models, uniquely capable of uncovering hidden genomic complexity, resolving aberrant phenotypes, and enhancing the reliability of in vivo disease modelling.

genomics↗

Hookworm genomic diversity and population structure from accessible sample types: A validated approach to generate genome-wide polymorphism datasets from individual third-stage larvae

Hookworm infection is a neglected tropical disease affecting hundreds of thousands of people annually in the tropics and sub-tropics. Population genomic approaches have the potential to improve our understanding of hookworm infection dynamics and control efficacy. Here, we validate an approach to generate genome-wide polymorphism datasets from accessible sample types in the zoonotic hookworm (Ancylostoma ceylanicum) then apply the validated approach in the human hookworm (Necator americanus) to compare laboratory- and field-derived samples. We first present an optimized method for purifying nucleic acid from individual third-stage hookworm larvae (L3s). We then measure the accuracy of variant call datasets generated through whole genome amplification (WGA) and next-generation sequencing (NGS). We demonstrate that WGA via multiple displacement amplification (MDA) introduces predictable biases that are exacerbated by low inputs and poor sample preservation but show that with sufficient input mass ([≥]0.1ng) we are still able to produce highly accurate variant call datasets from nucleic acid concentrations that reflect those of individual L3s. Using our validated approach, we infer laboratory- and field-collected samples of N. americanus as distinct populations, with higher levels of heterozygosity and nucleotide diversity identified in field-collected samples, suggesting signatures of inbreeding and/or drift are detectable in laboratory specimens within several years of initiation of infection. We also show that, despite expected reductions in heterozygosity, laboratory samples still possess numerous heterozygous sites, and we demonstrate that a reference genome generated from an adult worm from an early laboratory passage performs well for variant calling in both laboratory- and field-derived samples. Moving forward, our optimized method for nucleic acid purification can be broadly applied to generate input for any amplification-based approach where sequencing individual hookworm L3s, rather than a pool of specimens, is preferred. Our validated population genomics workflow can be used to characterize structure and connectivity of hookworm populations in endemic communities, with the goal of leveraging these insights to improve our approach to hookworm treatment and control. AUTHOR SUMMARYInfection with the human hookworm, Necator americanus, is a significant cause of morbidity in the global south. Population genomic techniques have the potential to improve our understanding of hookworm infection and control. However, third-stage larvae, or L3, which are the hookworm life-cycle stage we routinely have access to when screening infected people, are less than a millimeter long, and this small size makes generating genomic datasets from individual worms difficult. Here, we introduce an optimized approach for purifying DNA from individual L3s and validate its use with whole genome amplification (WGA) for population genomics. We found that WGA from L3s produces sequencing datasets that are biased in their breadth and depth of coverage across the hookworm genome. But by ensuring a minimum threshold for the mass of DNA input to WGA and setting strict criteria for variant filtration, these biases can be overcome to produce highly accurate variant calls genome-wide. We then use this approach to demonstrate reduced genetic diversity in a recently established laboratory hookworm strain as compared to field-collected samples. Our study outlines a specimen-through-analysis workflow that can be used with accessible sample types to measure population structure and diversity of hookworms in endemic communities.

genomics↗

Trypanosome histone variants H3.V and H4.V promote nucleosome plasticity in repressed chromatin.

Histone variants define distinct chromatin states by modulating the biophysical properties of nucleosomes. Variants play a particularly important role in the parasitic protist Trypanosoma brucei, which has unusual chromatin and lacks a canonical repressive heterochromatin system. Instead, T. brucei utilises specialised divergent histone variants H3.V and H4.V. However, the biochemical basis of their repressive functions is unknown. Here, we determined the structure of the H3.V-H4.V nucleosome core particle and biochemically characterised variant-containing nucleosomes and nucleosome arrays probing their unique properties. We discovered that surprisingly for repressive-state nucleosomes, H3.V promotes pronounced DNA splaying, largely via its N-terminal tail region, whilst retaining overall stability that is comparable to canonical nucleosomes. In contrast, H4.V exhibits near-identical binding to DNA but mediates a slight increase in histone octamer stability. The surface of the H3.V-H4.V nucleosome is altered and provides a differential platform for chromatin binding proteins, linking the variants to parasite pathogenicity.

biochemistry↗

ARP2/3 complex mediates the neuropathology of PTEN-deficient human neural cells downstream of mTORC1 and mTORC2 hyperactivation

Mutations in the phosphatase and tensin homolog (PTEN) gene are linked to severe neurodevelopmental disorders. Loss of PTEN causes hyperactivation of both mechanistic target of rapamycin (mTOR) complexes, mTORC1 and mTORC2. Recent studies have shown that this dual hyperactivation is required for the neuropathology observed in PTEN-deficient human stem cell-derived neural cells. However, the molecular effectors that integrate these synergistic signals remain unknown. Here, we identify the actin-regulating ARP2/3 complex as a critical point of convergence downstream of mTORC1 and mTORC2. We show that concurrent hyperactivation of both complexes drives increased filamentous actin and elevated levels of the ARP2/3 complex subunits in PTEN-deficient human neural precursors and neurons. Pharmacological or genetic inhibition of ARP2/3 is sufficient to rescue multiple disease-relevant phenotypes, including neural precursor hyperproliferation, neuronal hypertrophy, and electrical hyperactivity, without affecting the upstream mTORC1 or mTORC2 hyperactivation. Together, these findings reveal the PTEN-mTOR-ARP2/3 signaling axis as a core mechanism of neuropathology and highlight ARP2/3 inhibition as a potential therapeutic strategy for PTEN-related neurodevelopmental disorders.

neuroscience↗

MeCP2 requires interactions with nucleosome linker DNA to read chromatin DNA methylation

Methyl-CpG-binding protein 2 (MeCP2) is an epigenetic reader essential for neuronal function, but how it binds DNA methylation within chromatin is unclear. Using designer nucleosomes we observe that MeCP2 preferentially engages DNA methylation positioned at multiple sites around the nucleosome. Surprisingly, MeCP2 can bind methylated DNA in bent, histone-contacting core nucleosomal DNA. However, this activity requires additional DNA linker interactions, using MeCP2 regions beyond its canonical methyl binding domain. We mapped a novel DNA-binding region in MeCP2 required for this function. Furthermore, histone H1 antagonises the MeCP2-nucleosome interaction by competing for linker DNA. Overall, this reveals that MeCP2 combines nonspecific but essential interactions with linker DNA to aid specific binding to nucleosomal methylated DNA, independent of nucleosome structure. Our findings reveal a novel contribution to full MeCP2 function, and mechanistic insight into how this clinically important protein interacts with chromatin.

biochemistry↗

Chromatin Protection by the Chromosomal Passenger Complex

The chromosomal passenger complex (CPC; Borealin-Survivin-INCENP-Aurora B kinase) ensures accurate chromosome segregation by orchestrating sister chromatid cohesion, error-correction of kinetochore-microtubule attachments and spindle assembly checkpoint. Correct spatiotemporal regulation of CPC localization is critical for its function. Phosphorylations of Histone H3 Thr3 and Histone H2A Thr120 and modification-independent nucleosome interactions involving Survivin and Borealin contribute to CPC centromere enrichment. However, mechanistic basis for how various nucleosome binding elements collectively contribute to CPC centromere enrichment and whether CPC has any non-catalytic role at centromere remain open questions. Combining a high-resolution cryoEM structure of CPC-bound H3Thr3ph nucleosome with atomic force microscopy and biochemical and cellular assays, we demonstrate that CPC employs multipartite interactions involving both static and dynamic interactions, which facilitate its engagement at nucleosome acidic patch and DNA entry-exit site. Perturbing the CPC-nucleosome interaction compromises protection against MNase digestion in vitro, as well as the dynamic centromere association of CPC and centromeric chromatin stability in cells. Our work provides a mechanistic basis for the previously unexplained non-catalytic role of CPC in maintaining centromeric chromatin critical for kinetochore function.

biochemistry↗

Fat cadherin cleavage releases a transcriptionally active nuclear fragment to regulate target gene expression

The conserved atypical cadherin fat (ft) controls cellular processes such as growth, planar cell polarity, and mitochondrial function, in organisms ranging from fruit flies to mammals. Working at the apical-junctional plasma membrane the intracellular domain of the Ft protein, FtICD, binds to and regulates components of the Hippo and PCP pathways. Unexpectedly, we show that FtICD is present in the nucleus in cultured cells as well as in embryonic and larval tissues, and identify nuclear localization and nuclear export signals in FtICD required for this localization. We show that membrane-bound FtICD is cleaved and enters nuclei in vivo. Using endogenously tagged Ft as well as overexpressed FtICD we conducted ChIP-seq experiments and identified putative Ft targets including genes involved in signaling pathways, chromatin organization, pattern formation, and neural development. RNAseq demonstrates that some of these genes are differentially regulated in ft mutants. We observe strong correlations of Ft binding regions with peaks for other factors such as DREF and BEAF-32, as well as the Hpo pathway components Yorkie (Yki) and Scalloped (Sd), suggesting that Ft may act in conjunction with these factors to regulate gene expression. Supporting this hypothesis, we found that Ft can physically interact with both Yki and Sd in co-immunoprecipitation experiments in S2 cells. We propose that the modulation of Hippo pathway activity constitutes one of the nuclear functions of Ft, complementing its established function as an upstream regulator of Hippo signaling.

developmental biology↗

Two Key Actinomycetota Taxa in the Human Gut Microbiota are Associated with Schistosoma mansoni Infection Burden

In this study, we sought to identify key microbial taxa associated with human gut dysbiosis during S. mansoni infection and whether the changes are linked to the intensity of helminth infection. Stool samples were obtained from 20 persons infected with schistosomiasis and an equal number of uninfected persons from an endemic rural community in Ghana. Infection intensity was scored as egg count per gram (EPG) using the Kato-Katz method. Positive stool samples were further stratified as low-moderate (<400 EPG, n=15) and high (>400 EPG, n=5) infection burden. The composition and diversity of the gut microbiota and potential microbial markers associated with S. mansoni infection intensity were determined from 16S rRNA amplicon sequence analyses. No difference in {beta}-diversity was observed between positives and negatives (PERMANOVA: R2= 0.012, p= 0.723), although there was an increased abundance of Bifidobacterium (p= 0.008) in infected stool samples compared to the negatives. Further analyses showed that Bifidobacterium (p= 0.003) and Collinsella (p= 0.029) were elevated considerably among the low-moderate infected samples, while the pathobiont Escherichia-Shigella was reduced (p= 0.0078). Our findings show that intestinal schistosomiasis results in human gut microbiota dysbiosis, which is only distinguished when the intensity of infection is considered, with two key Actinomycetota species assuming importance depending on the infection burden. Author SummaryThis study investigates the relationship between Schistosoma mansoni infections, a major cause of intestinal schistosomiasis, and the human gut microbiome. Using samples from an endemic region in Ghana, the research examines how infection intensity impacts gut bacteria. The findings reveal that certain beneficial bacteria, such as Bifidobacterium and Collinsella, become more abundant in cases of low to moderate infection, potentially maintaining immune regulation and gut health. However, these effects are not seen in high-infection instances, possibly due to the aggressive hallmarks of high-intensity helminth infections. Understanding these dynamics could be pivotal for developing microbiome-based interventions to improve treatment outcomes for schistosomiasis and similar parasitic infections. This study sheds light on the complex interplay between infectious parasites and gut microbes, emphasising the promise of microbiome research in enhancing public health efforts in areas where parasitic diseases persist.

genomics↗

An updated reference genome sequence and annotation reveals gene losses and gains underlying naked mole-rat biology

The naked mole-rat (NMR; Heterocephalus glaber) is a eusocial subterranean rodent with a highly unusual set of physiological traits that has attracted great interest amongst the scientific community. However, the genetic basis of most of these traits has not been elucidated. To facilitate our understanding of the molecular mechanisms underlying NMR physiology and behaviour, we generated a long-read chromosomal-level genome assembly of the NMR. This genome was subsequently annotated and incorporated into multiple whole genome alignments in the Ensembl database. Our long-read assembly identified thousands of repeats and genes that were previously unassembled in the NMR and improved the results of routinely used short-read sequencing-based experiments such as RNA-seq, snRNA-seq, and ATAC-seq. We identified several spermatozoa related gene losses that may underlie the unique degenerative sperm phenotype in NMRs (IRGC, FSCB, AKAP3, MROH2B, CATSPER1, DCDC2C, ATP1A4, TEKT5, and ZAN), and an additional gene loss related to the established NK-cell absence in NMRs (PILRB). We resolved several tandem duplications in genes related to pathways underlying unique NMR adaptations including hypoxia tolerance, oxidative stress, and nervous system protection (TINF2, TCP1, KYAT1). Lastly, we describe our ongoing efforts to generate a reference telomere-to-telomere assembly in the NMR which includes the resolution of complex gene families. This new reference genome should accelerate the discovery of the genetic underpinnings of NMR physiology and adaptation.

genomics↗

Topoisomerase IIb binding underlies frequently mutated elements in cancer genomes

Type-II topoisomerases resolve topological stress in DNA through controlled double-strand breaks. While TOP2A is a chemotherapy target in proliferating cells, the ubiquitously expressed TOP2B is a potential off-target. Here we explore roles of TOP2B in mutagenesis by generating DNA-binding maps of TOP2B, CTCF, and RAD21 in human cancer samples and analysing these maps for driver mutations and mutational processes in 6500 whole cancer genomes. TOP2B-CTCF-RAD21 and TOP2B-RAD21 sites are enriched in somatic mutations and structural variants (SVs), especially at evolutionary conserved sites displaying high transcription and long-range chromatin interactions. TOP2B binding underlies SVs and hotspot mutations in cancer-driving genes such as TP53, MYC, FOXA1, and VHL, and many cis-regulatory elements. We show that the TOP2B-bound mutational hotspot at RMRP drives tumor initiation and growth in vivo. These data highlight TOP2B as a protector of the genome from topological challenges whose aberrant activity promotes driver and passenger mutations in cancer genomes.

cancer biology↗

C9orf72 expansion creates the unstable folate-sensitive fragile site FRA9A

The hyper-unstable Chr9p21 locus, harbouring the interferon gene cluster, oncogenes and C9orf72, is linked to multiple diseases. C9orf72 (GGGGCC)n expansions (C9orf72Exp) are associated with incompletely penetrant amyotrophic lateral sclerosis, frontotemporal dementia and autoimmune disorders. C9orf72Exp patients display hyperactive cGAS-STING-linked interferon immune and DNA damage responses, but the source of immuno-stimulatory or damaged DNA is unknown. Here, we show C9orf72Exp in pre-symptomatic and ALS-FTD patient cells and brains cause the folate- sensitive chromosomal fragile site, FRA9A. FRA9A centers on >33kb of C9orf72 as highly-compacted chromatin embedded in an 8.2Mb fragility zone spanning 9p21, encompassing 46 genes, making FRA9A one of the largest fragile sites. C9orf72Exp cells show chromosomal instability, heightened global- and Chr9p-enriched sister-chromatid exchanges, truncated-Chr9s, acentric-Chr9s and Chr9-containing micronuclei, providing endogenous sources of damaged and immunostimulatory DNA. Cells from one C9orf72Exp patient contained highly-rearranged FRA9A-expressing Chr9 with Chr9-wide dysregulated gene expression. Somatic C9orf72Exp repeat instability and chromosomal fragility are sensitive to folate-deficiency. Age-dependent repeat instability, chromosomal fragility, and chromosomal instability can be transferred to CNS and peripheral tissues of transgenic C9orf72Exp mice, implicating C9orf72Exp as the source. Our results highlight unappreciated effects of C9orf72 expansions that trigger vitamin-sensitive chromosome fragility, adding structural variations to the disease-enriched 9p21 locus, and likely elsewhere. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=94 SRC="FIGDIR/small/620312v2_ufig1.gif" ALT="Figure 1"> View larger version (31K): org.highwire.dtl.DTLVardef@154b23borg.highwire.dtl.DTLVardef@1814a6dorg.highwire.dtl.DTLVardef@13d713eorg.highwire.dtl.DTLVardef@d5d994_HPS_FORMAT_FIGEXP M_FIG C_FIG

genetics↗

The kinetoplastid kinetochore protein KKT23 acetyltransferase is a structural homolog of GCN5 that acetylates the histone H2A C-terminal tail

The kinetochore is the macromolecular protein machine that drives chromosome segregation in eukaryotes. In an evolutionarily divergent group of organisms called kinetoplastids, kinetochores are built using a unique set of proteins (KKT1-25 and KKIP1-12). KKT23 is a constitutively localised kinetochore protein containing a C-terminal acetyltransferase domain of unknown function. Here, using X-ray crystallography and NMR spectroscopy, we have determined the structure and dynamics of the KKT23 acetyltransferase domain from Trypanosoma brucei and found that it is structurally similar to the GCN5 histone acetyltransferase domain. We find that KKT23 can acetylate the C-terminal tail of histone H2A and that knockdown of KKT23 results in decreased H2A acetylation levels in T. brucei. Finally, we have determined the crystal structure of the N-terminal region of KKT23 and shown that it interacts with KKT22. Our study provides important insights into the structure and function of the unique kinetochore acetyltransferase in trypanosomes.

cell biology↗

The N-terminal region of DNMT3A combines multiple chromatin reading motifs to guide recruitment.

DNA methyltransferase 3A (DNMT3A) plays a critical role in establishing and maintaining DNA methylation patterns. However, the mechanisms underlying DNMT3A recruitment to and function within different chromatin environments remain unclear. Using a combination of biochemical and structural approaches we find that DNMT3A interacts using multiple interfaces with chromatin; directly binding generic nucleosome features as well as site-specific post-translational histone modifications. The N-terminal region, unique to the DNMT3A1 isoform, is essential for these interactions and stabilises H3K36me2-nucleosome recruitment. Intriguingly, in the same region critical for nucleosome binding we also map a ubiquitylation-dependent recruitment motif (UDR). The UDR binds specifically to ubiquitylated H2AK119, explaining the previously observed recruitment to Polycomb-occupied heterochromatin. A cryo-EM structure of DNMT3A1-DNMT3L with a modified nucleosome reveals that the UDR interacts with the nucleosome surface including the acidic patch. Previously unexplained disease-associated mutations are present in the UDR and ablate nucleosome interactions. This leads to an increased understanding of how DNMT3A1 recruitment occurs in the genome and highlights the importance of multivalent binding of DNMT3A to histone modifications and the nucleosome.

biochemistry↗

Age, sex, and cell type-resolved hypothalamic gene expression across the pubertal transition in mice

Although the hypothalamus plays a critical role in the regulation of puberty, more research is needed to identify the gene regulatory networks that control pubertal timing. Here, we investigate the age-, sex- and cell-type-specific gene regulation in the hypothalamus across the pubertal transition. We used RNA-seq to profile hypothalamic gene expression in male and female mice at five time points spanning the onset of puberty (postnatal days (PD) 12, 22, 27, 32, and 37). By combining this data with hypothalamic scRNA-seq data of pre- and post-pubertal mice, we were able to assign gene expression changes to their cell types of origin. In our colony, pubertal onset occurs earlier in male mice allowing us to focus on genes whose expression is dynamic across ages and offset between sexes and to explore bases of sex effects. Our age-by- sex pattern of expression enriched for biological pathways involved hormone production, neuronal activation, and glial maturation. Additionally, we found a dramatic expansion of oligodendrocytes precursor cells into mature oligodendrocytes spanning the pre-pubertal (PD12) to peri-pubertal (PD27) timepoints, and that genes driving this expansion enrich for genes involved in pubertal regulation. Together, by incorporating multiple biological timepoints with male and female mice simultaneously, our work furthers the understanding of gene and cell-type changes that accompany the development of secondary sex characteristics in both sexes.

genomics↗

Histone divergence in Trypanosoma brucei results in unique alterations to nucleosome structure

Eukaryotes have a multitude of diverse mechanisms for organising and using their genomes, but the histones that make up chromatin are highly conserved. Unusually, histones from kinetoplastids are highly divergent. The structural and functional consequences of this variation are unknown. Here, we have biochemically and structurally characterised nucleosome core particles (NCPs) from the kinetoplastid parasite Trypanosoma brucei. A structure of the T. brucei NCP reveals that global histone architecture is conserved, but specific sequence alterations lead to distinct DNA and protein interaction interfaces. The T. brucei NCP is unstable and has weakened overall DNA binding. However, dramatic changes at the H2A-H2B interface introduce local reinforcement of DNA contacts. The T. brucei acidic patch has altered topology and is refractory to known binders, indicating that the nature of chromatin interactions in T. brucei may be unique. Overall, our results provide a detailed molecular basis for understanding evolutionary divergence in chromatin structure.

biochemistry↗

BRCA1-BARD1 combines multiple chromatin recognition modules to bridge nascent nucleosomes

Chromatin association of the BRCA1-BARD1 heterodimer is critical to promote homologous recombination repair of DNA double-strand breaks (DSBs) in S/G2. How the BRCA1-BARD1 complex interacts with chromatin that contains both damage induced histone H2A ubiquitin and inhibitory H4AK20 methylation is not fully understood. We characterised BRCA1-BARD1 binding and enzymatic activity to an array of mono- and di-nucleosome substrates using biochemical, structural, and single molecule imaging approaches. We find that the BRCA1-BARD1 complex preferentially interacts and modifies di-nucleosomes over mono-nucleosomes, allowing integration of H2A Lys-15 ubiquitylation signals with other chromatin modifications and features. Using high speed-AFM to provide real-time visualization of BRCA1-BARD1 complex recognising chromatin, we show a highly dynamic complex that bridges two nucleosomes and associates with the DNA linker region. Bridging is aided by multivalent cross-nucleosome interactions that enhance BRCA1-BARD1 E3 ubiqiutin ligase catalytic activity. Multivalent interactions across nucleosomes explains how BRCA1-BARD1 can recognize chromatin that retains partial di-methylation at H4 Lys-20 (H4K20me2), a parental histone mark that blocks BRCA1-BARD1 interaction with nucleosomes, to promote its enzymatic and DNA repair activities.

molecular biology↗

Transcriptional buffering and 3'UTR lengthening are shaped during human neurodevelopment by shifts in mRNA stability and microRNA load

The contribution of mRNA half-life is commonly overlooked when examining changes in mRNA abundance during development. mRNA levels are regulated by transcription rate or mRNA half-life, but combinations of both could boost or buffer the final steady-state. We measured transcription rate and mRNA half-life changes during human induced pluripotent stem cell (iPSC)-derived neuronal development using RATE-seq. The most prevalent mode of gene regulation during transitions to neuronal progenitors and neurons was transcriptional buffering. Less prevalent modes consisted of transcriptional boosting events, transcription rate only shifts, or mRNA half-life only shifts. Buffered and novel boosted gene sets were enriched in RNA-binding protein (RBP) motifs and microRNA sites. Global mRNA half-life decreased two-fold in neurons. microRNA copy number per cell increased during neurodevelopment coincident with destabilization of a subset of short isoforms that contributed to increased average 3'UTR length. Our findings identify mRNA instability mechanisms that regulate transcript levels and 3'UTR isoform abundance, and provide a precedent for transcriptional boosting or buffering during development of other human tissues.

molecular biology↗