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Conrad, D. F.

Publications and source records attributed to Conrad, D. F..

13 recordsLinked to original sources

PRDM9-mediated meiotic hotspot specification is constrained in humans despite extensive sequence diversity

PRDM9 specifies meiotic recombination hotspots through a rapidly evolving C2H2 zinc-finger (ZNF) coding minisatellite that determines DNA-binding specificity. Although this minisatellite harbors extraordinary allelic diversity in humans, the functional consequences of most naturally occurring variants remain unknown. Here we functionally characterize 80 human PRDM9 alleles using genome-wide chromatin profiling. Despite extensive sequence diversity within the ZNF array, most alleles function indistinguishably from common A and C hotspot-specifying alleles, revealing that human PRDM9 function is more constrained than its sequence diversity predicts. In contrast, rare and infertility-associated variants occupy two functional extremes: either abundant and novel DNA binding specificity or minimal DNA binding, suggesting that both gain- and loss-of-function alleles may disrupt symmetric hotspot specification during meiosis, thus representing a plausible contributor to human infertility. Together, our findings define the functional landscape of human PRDM9 variation and provide a framework for interpreting the impact of newly discovered PRDM9 alleles.

genomics↗

Census and genetic analysis of the United States marmoset population

The common marmoset (Callithrix jacchus), a small monkey native to Brazil, has been used as a biomedical model in the United States (US) since the 1950s, yet the origins, genomic diversity, and population structure of current colonies remain poorly defined. Through the NIH Marmoset Coordinating Center, we registered and sampled most US research marmosets ([~]2,300 living animals) and assembled pedigrees and historical records for >10,000 individuals. We present a resource of >800 whole-genome sequences, largely from US colonies. These data reveal an unexpected population structure that predates the establishment of research colonies. Indeed, this population structure mirrors variation found in marmosets across Brazil. Leveraging sequenced families, we generate the first pedigree-based recombination map and improved estimates of de novo mutation processes for this species. Our insights into genetic diversity, structure, and inbreeding will guide colony management, inform disease modelling and strengthen the marmosets standing as a biomedical model. Further, this work demonstrates how coordinated efforts across colonies can enable a self-sustaining "living laboratory", supporting data sharing and well-powered studies beyond the reach of single institutions.

genetics↗

A Complete Genome for the Common Marmoset

The common marmoset is a New World monkey (NWM) commonly used as a model organism to investigate questions in primate evolution and human disease, including Alzheimers and other neurodegenerative diseases, as well as neuropsychiatric disorders. Here we present the first telomere-to-telomere (T2T) reference genome for the common marmoset, adding over 88 Mb of sequence and resolving challenging genomic regions. An additional near-T2T assembly from a second unrelated individual yields a total of four high-quality haplotypes for analysis. The improved contiguity and accuracy of these assemblies enable unprecedented insights into complex and rapidly evolving genomic regions such as centromeres, sex chromosomes, ribosomal DNA (rDNA) structure, and the major histocompatibility complex (MHC). We fully resolved all marmoset centromeres, uncovering dimeric alpha satellites with chromosomal specificity and stratified inactive layers documenting ancestral centromere turnover. We assembled six acrocentric autosomes with gene-poor, satellite-rich short arms and provide evidence that most of them can harbor rDNA and all of them share large pseudo-homologous regions (PHRs). The Y chromosome, but not the X chromosome, carries active rDNA and PHRs, and the rDNA copy number is sexually dimorphic. Chromosomes that share PHRs also share closely related centromeric satellite DNA, supporting a model of ongoing recombinational exchange between heterologous chromosomes facilitated by rDNA. We discovered multiple novel, marmoset-specific MHC genes that are predicted to protect against pathogens encountered in its environment. Leveraging this complete reference, we further identified over 500 transcribed genes with transcript models or expansions specific to the marmoset lineage. Together with additional long-read marmoset assemblies, these genomes were used to construct a marmoset pangenome, providing a robust reference framework for short-read mapping across diverse individuals. This resource will improve the utility of the common marmoset as a biomedical model organism and fill key gaps in our understanding of primate evolution.

genomics↗

A novel CCDC112-dependent process of sperm midpiece formation and epididymal maturation

The sperm mitochondrial sheath has proposed functions in structural support and energy production for motility. Here we define coiled coil domain containing protein 112, CCDC112, as crucial for male fertility, specifically in the assembly and function of the mitochondrial sheath. We unveiled a previously unrecognised process of epididymal mitochondrial sheath maturation. Sperm mitochondrial sheaths are structurally immature upon exiting the testis and continue to mature as they transit from the caput to the cauda epididymis. Data reveal the critical role of CCDC112 in mitochondrial morphogenesis during sheath formation. A lack of CCDC112 lead to significantly reduced mitochondrial respiration capacity, irregular flagellar waveforms, diminished progressive motility and a failure of sperm to traverse the female reproductive tract to the site of fertilisation and penetrate the zonae pellucidae of oocytes. Finally, we identify CCDC112 as a component of the distal appendages of the mother centriole and identify a facilitative role in core tail assembly. Collectively, CCDC112 is a key regulator of sperm mitochondrial sheath assembly while further expanding the understanding of spermatogenesis, energy generation and flagella kinematics.

developmental biology↗

PSAP-genomic-regions: a method leveraging population data to prioritize coding and non-coding variants in whole genome sequencing for rare disease diagnosis

The introduction of next generation sequencing technologies in the clinics has improved rare disease diagnosis. Nonetheless, for very heterogeneous or very rare diseases, more than half of cases still lack molecular diagnosis. Novel strategies are needed to prioritize variants within a single individual. The PSAP (Population Sampling Probability) method was developed to meet this aim but only for coding variants in exome data. To address the challenge of the analysis of non-coding variants in whole genome sequencing data, we propose an extension of the PSAP method to the non-coding genome called PSAP-genomic-regions. In this extension, instead of considering genes as testing units (PSAP-genes strategy), we use genomic regions defined over the whole genome that pinpoint potential functional constraints. We conceived an evaluation protocol for our method using artificially-generated disease exomes and genomes, by inserting coding and non-coding pathogenic ClinVar variants in large datasets of exomes and genomes from the general population. We found that PSAP-genomic-regions significantly improves the ranking of these variants compared to using a pathogenicity score alone. Using PSAP-genomic-regions, more than fifty percent of non-coding ClinVar variants, especially those involved in splicing, were among the top 10 variants of the genome. In addition, our approach gave similar results compared to PSAP-genes regarding the scoring of coding variants. On real sequencing data from 6 patients with Cerebral Small Vessel Disease and 9 patients with male infertility, all causal variants were ranked in the top 100 variants with PSAP-genomic-regions. By revisiting the testing units used in the PSAP method to include non-coding variants, we have developed PSAP-genomic-regions, an efficient whole-genome prioritization tool which offers promising results for the diagnosis of unresolved rare diseases. PSAP-genomic-regions is implemented as a user-friendly Snakemake workflow, accessible to both researchers and clinicians which can easily integrate up-to-date annotation from large databases. Author summaryIn recent years, improvement in DNA sequencing technologies has allowed the identification of many genes involved in rare diseases. Nonetheless, the molecular diagnosis is still unknown for more than half of rare diseases cases. This is in part due to the large heterogeneity of molecular causes in rare diseases. This also highlights the need for the development of new methods to prioritize pathogenic variants from DNA sequencing data at the scale of the whole genome and not only coding regions. With PSAP-genomic-regions, we offer a strategy to prioritize coding and non-coding variants in whole-genome data from a single individual in need of a diagnosis. The PSAP-genomic-regions combines information on the predicted pathogenicity and frequency of variants in the context of functional regions of the genome. In this work, we compare the PSAP-genomic-regions strategy to other variant prioritization strategies on simulated and real data. We show the better performance of PSAP-genomic-regions over a classical approach based on variant pathogenicity scores alone. PSAP-genomic-regions provides a straightforward approach to prioritize causal pathogenic variants, especially non-coding ones, that are often missed with other strategies and could explain the cause of undiagnosed rare diseases.

genetics↗

Taking identity-by-descent analysis into the wild: Estimating realized relatedness in free-ranging macaques

Biological relatedness is a key consideration in studies of behavior, population structure, and trait evolution. Except for parent-offspring dyads, pedigrees capture relatedness imperfectly. The number and length of DNA segments that are identical-by-descent (IBD) yield the most precise estimates of relatedness. Here, we leverage novel methods for estimating locus-specific IBD from low coverage whole genome resequencing data to demonstrate the feasibility and value of resolving fine-scaled gradients of relatedness in free-living animals. Using primarily 4-6x coverage data from a rhesus macaque (Macaca mulatta) population with available long-term pedigree data, we show that we can call the number and length of IBD segments across the genome with high accuracy even at 0.5x coverage. The resulting estimates demonstrate substantial variation in genetic relatedness within kin classes, leading to overlapping distributions between kin classes. They identify cryptic genetic relatives that are not represented in the pedigree and reveal elevated recombination rates in females relative to males, which allows us to discriminate maternal and paternal kin using genotype data alone. Our findings represent a breakthrough in the ability to understand the predictors and consequences of genetic relatedness in natural populations, contributing to our understanding of a fundamental component of population structure in the wild.

ecology↗

CEP76 is a critical regulator of male germ cell transition zone function and tail composition

The transition zone is a specialised gate at the base of cilia/flagella, which segregates the ciliary compartment from the cytoplasm and strictly regulates protein entry. In this study, we have identified CEP76 as an essential germ cell transition zone protein, involved in the selective entry and incorporation of key proteins required for sperm function and fertility into the ciliary compartment and ultimately the sperm tail. In its absence sperm tails are shorter and immotile as a consequence of deficits in essential sperm motility proteins including DNAH2 and AKAP4, which accumulate at the sperm neck in the mutant. We demonstrate CEP76 is required for sperm tail fibrous sheath formation, outer dense fibre loading and axoneme stability in the principal piece and ultimately sperm motility. Finally, we identify that CEP76 dictates annulus positioning and composition, adding further evidence that the spermatid transition zone and annulus are part of the same functional structure.

cell biology↗

TAD Evolutionary and functional characterization reveals diversity in mammalian TAD boundary properties and function

Topological associating domains (TADs) are self-interacting genomic units crucial for shaping gene regulation patterns. Despite their importance, the extent of their evolutionary conservation and its functional implications remain largely unknown. In this study, we generate Hi-C and ChIP-seq data and compare TAD organization across four primate and four rodent species, and characterize the genetic and epigenetic properties of TAD boundaries in correspondence to their evolutionary conservation. We find that only 14% of all human TAD boundaries are shared among all eight species (ultraconserved), while 15% are human-specific. Ultraconserved TAD boundaries have stronger insulation strength, CTCF binding, and enrichment of older retrotransposons, compared to species-specific boundaries. CRISPR-Cas9 knockouts of two ultraconserved boundaries in mouse models leads to tissue-specific gene expression changes and morphological phenotypes. Deletion of a human-specific boundary near the autism-related AUTS2 gene results in upregulation of this gene in neurons. Overall, our study provides pertinent TAD boundary evolutionary conservation annotations, and showcase the functional importance of TAD evolution.

evolutionary biology↗

The origins and functional effects of postzygotic mutations throughout the human lifespan

Postzygotic mutations (PZMs) begin to accrue in the human genome immediately after fertilization, but how and when PZMs affect development and lifetime health remains unclear. To study the origins and functional consequences of PZMs, we generated a multi-tissue atlas of PZMs from 948 donors using the final major release of the Genotype-Tissue Expression (GTEx) project. Nearly half the variation in mutation burden among tissue samples can be explained by measured technical and biological effects, while 9% can be attributed to donor-specific effects. Through phylogenetic reconstruction of PZMs, we find that their type and predicted functional impact varies during prenatal development, across tissues, and the germ cell lifecycle. Remarkably, a class of prenatal mutations was predicted to be more deleterious than any other category of genetic variation investigated and under positive selection as strong as somatic mutations in cancers. In total, the data indicate that PZMs can contribute to phenotypic variation throughout the human lifespan, and, to better understand the relationship between genotype and phenotype, we must broaden the long-held assumption of one genome per individual to multiple, dynamic genomes per individual. One-Sentence SummaryThe predicted rates, functional effects and selection pressure of postzygotic mutations vary through the human lifecycle.

genomics↗

Biallelic mutations in M1AP are a frequent cause of meiotic arrest leading to male infertility

Male infertility affects [~]7% of men in Western societies, but its causes remain poorly understood. The most clinically severe form of male infertility is non-obstructive azoospermia (NOA), which is, in part, caused by an arrest at meiosis, but so far only few genes have been reported to cause germ cell arrest in males. To address this gap, whole exome sequencing was performed in 60 German men with complete meiotic arrest, and we identified in three unrelated men the same homozygous frameshift variant c.676dup (p.Trp226LeufsTer4) in M1AP, encoding meiosis 1 arresting protein. Then, with collaborators from the International Male Infertility Genomics Consortium (IMIGC), we screened a Dutch cohort comprising 99 infertile men and detected the same homozygous variant c.676dup in a man with hypospermatogenesis predominantly displaying meiotic arrest. We also identified two Portuguese men with NOA carrying likely biallelic loss-of-function (LoF) and missense variants in M1AP among men screened by the Genetics of Male Infertility Initiative (GEMINI). Moreover, we discovered a homozygous missense variant p.(Pro389Leu) in M1AP in a consanguineous Turkish family comprising five infertile men. M1AP is predominantly expressed in human and mouse spermatogonia up to secondary spermatocytes and previous studies have shown that knockout male mice are infertile due to meiotic arrest. Collectively, these findings demonstrate that both LoF and missense M1AP variants that impair its protein cause autosomal-recessive meiotic arrest, non-obstructive azoospermia and male infertility. In view of the evidence from several independent groups and populations, M1AP should be included in the growing list of validated NOA genes.

genetics↗

The genetic architecture of sporadic and recurrent miscarriage

Miscarriage is a common complex trait that affects 10-25% of clinically confirmed pregnancies1,2. Here we present the first large-scale genetic association analyses with 69,118 cases from five different ancestries for sporadic miscarriage and 750 cases of European ancestry for recurrent miscarriage, and up to 359,469 female controls. We identify one genome-wide significant association on chromosome 13 (rs146350366, minor allele frequency (MAF) 1.2%, Pmeta=3.2x -8 (CI) 1.2-1.6) for sporadic miscarriage in our European ancestry meta-analysis (50,060 cases and 174,109 controls), located near FGF9 involved in pregnancy maintenance3 and progesterone production4. Additionally, we identified three genome-wide significant associations for recurrent miscarriage, including a signal on chromosome 9 (rs7859844, MAF=6.4%, Pmeta=1.3x -8 in controlling extravillous trophoblast motility5. We further investigate the genetic architecture of miscarriage with biobank-scale Mendelian randomization, heritability and, genetic correlation analyses. Our results implicate that miscarriage etiopathogenesis is partly driven by genetic variation related to gonadotropin regulation, placental biology and progesterone production.

genetics↗

RegTools: Integrated analysis of genomic and transcriptomic data for discovery of splicing variants in cancer

Somatic mutations within non-coding regions and even exons may have unidentified regulatory consequences that are often overlooked in analysis workflows. Here we present RegTools (www.regtools.org), a computationally efficient, free, and open-source software package designed to integrate somatic variants from genomic data with splice junctions from bulk or single cell transcriptomic data to identify variants that may cause aberrant splicing. RegTools was applied to over 9,000 tumor samples with both tumor DNA and RNA sequence data. We discovered 235,778 events where a splice-associated variant significantly increased the splicing of a particular junction, across 158,200 unique variants and 131,212 unique junctions. To characterize these somatic variants and their associated splice isoforms, we annotated them with the Variant Effect Predictor (VEP), SpliceAI, and Genotype-Tissue Expression (GTEx) junction counts and compared our results to other tools that integrate genomic and transcriptomic data. While many events were corroborated by the aforementioned tools, the flexibility of RegTools also allowed us to identify novel splice-associated variants and previously unreported patterns of splicing disruption in known cancer drivers, such as TP53, CDKN2A, and B2M, as well as in genes not previously considered cancer-relevant.

bioinformatics↗

Somatically Mutated Genes Under Positive and Negative Selection Found by Transcriptome Sequence Analysis Include Oncogene and Tumor Suppressor Candidates

IntroductionOncogenic somatic mutations confer proliferative advantage and undergo positive clonal selection. We developed software and applied new analytical approaches to identify: (1) somatic mutations in diverse tissues, (2) somatically mutated genes under positive and negative selection, (3) post-transcriptional modifications in the mitochondrial transcriptome, and (4) inherited germline alleles predisposing people to higher somatic mutation burden or higher levels of post-transcriptional modification.\n\nMethodsTranscriptome sequence data (Genotype Tissue Expression project) for 7051 tissue samples from 549 postmortem donors and representing 44 tissue types were used. Germline mutations were inferred from whole-exome DNA sequencing and SNP arrays. DNA somatic mutations were inferred from variant allele frequencies (VAF) in RNA-seq data. Post-transcriptional modifications were inferred from Polymorphism Information Content (PIC) at the p9 sites of mitochondrial tRNA sequences. Positive and negative clonal selection was evaluated using a nonsynonomous/synonomous mutation rate (dN/dS) model. Genome-wide association studies (GWAS) were assessed with mitochondrial PIC for post-transcriptional modification level, or using the total number of somatic mutations observed per donor for somatic mutation burden.\n\nResultsOur dN/dS model identified 78 genes under negative selection for somatic mutations (dN/dS < 1, padj < 0.05) and 14 under positive selection (dN/dS > 1, padj <0.05). Our GWAS identified 2 sites associated with post-transcriptional modification (1 approaching significance with p=5.99x10-8, 1 with p<5x10-8) and [~]20 sites associated with somatic mutation burden (p<5x10- 8).\n\nConclusionsTo our knowledge these are the first genome-wide association studies on normal somatic mutation burden. These studies were an attempt to increase understanding of the somatic mutation process. Our work identified somatic mutations at the global organismal level that may promote cell proliferation in a tissue-specific manner. By identifying tissue-specific mutations in actively expressed genes that appear before cancer phenotype is detected, this work also identifies gene candidates that might initiate tumorigenesis.

genomics↗