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Biology subjects

Williams, A. E.

Publications and source records attributed to Williams, A. E..

15 recordsLinked to original sources

Escape from replicative crisis and immortalization precedes complex genome evolution

Shortening of telomeres restricts the proliferative capacity of human somatic cells by inducing replicative senescence and crisis. During cancerous transformation, premalignant cells must overcome these barriers and acquire replicative immortality. Single-cell DNA strand-specific genome sequencing of crisis cells revealed extreme genome instability characterized by complex chromosomal abnormalities. Unexpectedly, spontaneously emerging postcrisis clones showed relatively few and simple structural variants. However, with accumulating divisions following crisis escape, the genomes of immortal postcrisis clones evolve and amass genomic alterations, including tetraploidization events with subsequent losses and gains of individual chromosomes. Our data point towards a new model of tumorigenesis in which crisis acts as a strong selective barrier against cells with aberrant karyotypes, and in which high karyotypic complexity is acquired after immortalization and crisis escape.

cell biology↗

Targeting CyclinD1-CDK6 to Mitigate Senescence-Driven Inflammation and Age-Associated Functional Decline

Cellular senescence contributes to aging and age-related diseases by driving chronic inflammation through the Senescence Associated Secretory Phenotype (SASP) and interferon-stimulated genes (ISGs). Cyclin D1 (CCND1), a key cell cycle regulator, is paradoxically upregulated in these non-proliferating cells. We show that CCND1 and its kinase partner CDK6 drive SASP and ISG expression in senescent cells by promoting DNA damage accumulation. This leads to the formation of cytoplasmic chromatin fragments (CCFs) that activate pro-inflammatory CGAS-STING signaling. The tumor suppressor p53 (TP53) and its target p21 (CDKN2A) antagonize this CCND1-CDK6-dependent DNA damage accumulation pathway to suppress the SASP. In aged mouse livers, senescent hepatocytes show increased Ccnd1 expression. Hepatocyte-specific Ccnd1 knockout or treatment with the Cdk4/6 inhibitor Palbociclib reduces DNA damage and ISGs in aged mouse liver. Notably, Palbociclib also suppresses frailty and improves physical performance of aged mice. These findings reveal a novel role for CCND1/CDK6 in regulating DNA damage and inflammation in senescence and aging, highlighting it as a promising therapeutic target.

cell biology↗

Med14 phosphorylation shapes genomic response to GLP-1 Agonist

Under feeding conditions, release of glucagon-like peptide (GLP-1) from intestinal L cells promotes insulin secretion and pancreatic beta cell viability. Binding of GLP-1 to its cognate receptor on the beta cell surface results in induction of the cAMP signaling pathway, leading to the protein kinase A (PKA) mediated phosphorylation of CREB and induction of CREB target genes. By contrast with the acute effects of this pathway on immediate early CREB target genes, which attenuate the cAMP-CREB response, sustained exposure of beta cells to the stable GLP-1 receptor agonist Exendin-4 stimulates the expression of beta cell specific CREB target genes with delayed kinetics. In a proteomic screen for transcriptional co-regulators that mediate the long-term effects of GLP-1 analogs, we identified Med14, a backbone subunit of the Mediator complex. Exposure to Exendin-4 stimulates Med14 phosphorylation at Ser983, corresponding to a conserved PKA recognition site (RRXS) that is located within an intrinsically disordered region of Med14. Phosphorylation of Med14 by PKA is essential for maintenance of enhancers that drive induction of beta cell-specific and diabetes-linked genes. Mutation of Med14 at Ser983 to alanine decreased beta cell numbers and repressed Exendin-4 induced gene regulation in primary mouse beta cells. Our work reveals how phosphorylation of a general transcription factor in response to GLP-1 analogs triggers a broad genomic response with salutary effects on beta cell function.

genomics↗

A single valine to leucine switch disrupts Plasmodium falciparum AP2-G DNA binding and reveals the role of GDV1 in ap2-g activation.

Sexual commitment in Plasmodium parasites is essential for malaria transmission, yet much remains unknown about the underlying signaling events initiating sexual conversion in a subpopulation of parasites. We discovered a single valine (V2163) to leucine (L2163) mutation in an Apetala 2 (AP2) transcription factor required for P. falciparum gametocytogenesis, ap2-g that abrogates sexual differentiation and confirmed this with forward and reverse mutation editing. Mutated AP2-G.L2163 does not bind the ap2-g consensus motif, GnGTAC, or stimulate AP2-G-dependent gene transcription including autoregulation. We then used AP2-G.L2163 parasite lines as tools to demonstrate the critical role of GDV1 in the initial activation of the silent ap2-g locus during the trophozoite to schizont transition in the absence of functional AP2-G and its autoregulation. Additionally, we show that AP2-G.V is required for MSRP1 expression, which can be used to distinguish early and late sexually committed schizonts. Together this work demonstrates that valine2163 in AP2-G plays a critical role in DNA binding, highlighting the functional importance of this specific region for malaria transmission as well as the critical role of GDV1 in the initial activation of ap2-g expression and induction of sexual differentiation. The reporter lines generated allow further study of signaling pathways or screening of factors regulating sexual commitment.

microbiology↗

Fusome morphogenesis is sufficient to promote female germline stem cell self-renewal in Drosophila

Germline cysts, or interconnected groups of germ cells, promote the synchronization of gamete development in vertebrates and invertebrates. In the Drosophila ovary, cyst formation is coordinated by the fusome, a unique endoplasmic reticulum-like organelle. Although many structural components of the fusome have been characterized, little is known about the genetic factors that control fusome growth and distribution between germ cells. Here, we identify the {beta}-importin, Tnpo-SR, as an important regulator of fusome morphogenesis in germline stem cells (GSCs) and their dividing daughters. Although Tnpo-SR does not aggregate at fusomes or centrosomes, Tnpo-SR null mutants fail to form proper fusomes and knock-down of Tnpo-SR reduces fusome accumulation, ultimately leading to cyst fragmentation and improper numbers of germ cells within an egg chamber. Tnpo-SR depletion disrupts microtubule organization during interphase and sub-cellular localization of the microtubule associated protein Asp. However, overexpression of asp is not sufficient to restore fusome size or cyst architecture when Tnpo-SR is depleted, suggesting that Tnpo-SR-dependent regulation of asp does not solely control fusome morphogenesis. Instead, we find that restoring fusome size by overexpressing the core fusome component hu-li tai shao or the polarity factor Par3/bazooka is sufficient to restore fusome area in Tnpo-SR-depleted GSCs. Moreover, restoration of fusome area in the absence of Tnpo-SR also rescues cyst organization and oocyte specification, suggesting that Tnpo-SR functions upstream of fusome structural component production. Taken together, these data functionally link nuclear import/export machinery to fusome morphogenesis during Drosophila germline cyst development. ARTICLE SUMMARYThe fusome plays a key role in cyst formation in the Drosophila ovarian germline, yet regulation of fusome growth and distribution between germ cells after mitosis remains understudied. Through loss-of-function analyses, the authors identify Tnpo-SR as a novel regulator of fusome morphogenesis. Tnpo-SR depletion reduces the core fusome structural component Hts in germline stem cells (GSCs) and disrupts microtubule organization and nucleation. Overexpression of Hts or Par3/bazooka in Tnpo-SR-depleted GSCs restores fusome size, which in turn rescues cyst organization and oocyte specification. These findings establish Tnpo-SR as an upstream regulator of Hts during fusome morphogenesis.

developmental biology↗

Global genomics of Aedes aegypti unveils widespread and novel persistent infectious viruses capable of triggering a small RNA response

The mosquito Aedes aegypti is a prominent vector for arboviruses, but the breadth of mosquito viruses that infects this specie is not fully understood. In the broadest global survey to date of over 200 Ae. aegypti small RNA samples, we detected viral small interfering RNAs (siRNAs) and Piwi interacting RNAs (piRNAs) arising from mosquito viruses. We confirmed that most academic laboratory colonies of Ae. aegypti lack persisting viruses, yet two commercial strains were infected by a novel tombus-like virus. Ae. aegypti from North to South American locations were also teeming with multiple insect viruses, with Anphevirus and a bunyavirus displaying geographical boundaries from the viral small RNA patterns. Asian Ae. aegypti small RNA patterns indicate infections by similar mosquito viruses from the Americas and reveal the first wild example of dengue virus infection generating viral small RNAs. African Ae. aegypti also contained various viral small RNAs including novel viruses only found in these African substrains. Intriguingly, viral long RNA patterns can differ from small RNA patterns, indicative of viral transcripts evading the mosquitoes RNA interference (RNAi) machinery. To determine whether the viruses we discovered via small RNA sequencing were replicating and transmissible, we infected C6/36 and Aag2 cells with Ae. aegypti homogenates. Through blind passaging, we generated cell lines stably infected by these mosquito viruses which then generated abundant viral siRNAs and piRNAs that resemble the native mosquito viral small RNA patterns. This mosquito small RNA genomics approach augments surveillance approaches for emerging infectious diseases.

genomics↗

PCBS: an R package for fast and accurate analysis of bisulfite sequencing data

MotivationWhole-genome bisulfite sequencing is a powerful tool for analyzing chromatin methylation genome-wide, but analysis of whole-genome bisulfite data is hampered by slow, inaccurate, and inflexible pipelines. ResultsWe developed PCBS, a computationally efficient R package for Whole Genome Bisulfite Sequencing analysis that demonstrates remarkable accuracy and flexibility compared to current tools. PCBS identifies differentially methylated loci and differentially methylated regions and offers novel functionality that allows for more targeted methylation analyses. PCBS uses minimal computational resources; a complete pipeline in mouse can run on a local RStudio instance in a matter of minutes. Availability and ImplementationPCBS is an R package available under a GNU GPLv3 license at: https://github.com/katlande/PCBS and from CRAN: https://CRAN.R-project.org/package=PCBS. Instructions for use are available at: https://katlande.github.io/PCBS/. Supplementary Information"Supplementary data are available on BioRXiv."

bioinformatics↗

Alterations in the Mammary Gland and Tumor Microenvironment of Formerly Obese Mice

Obesity is a risk factor for breast cancer, and women with obesity that develop breast cancer have a worsened prognosis. Within the mammary gland, obesity causes chronic, macrophage-driven inflammation and adipose tissue fibrosis. To examine the impact of weight loss on the mammary microenvironment, mice were fed high-fat diet to induce obesity, then switched to a low-fat diet. In formerly obese mice, we observed reduced numbers of crown-like structures and fibrocytes in mammary glands, while collagen deposition was not resolved with weight loss. Following transplant of TC2 tumor cells into the mammary glands of lean, obese, and formerly obese mice, diminished collagen deposition and cancer-associated fibroblasts were observed in tumors from formerly obese mice compared to obese mice. When TC2 tumor cells were mixed with CD11b+CD34+ myeloid progenitor cells, collagen deposition within the tumors was significantly greater compared to when tumor cells were mixed with CD11b+CD34- monocytes, suggesting that fibrocytes contribute to early collagen deposition in mammary tumors of obese mice. Overall, these studies show that weight loss resolved some of the microenvironmental conditions within the mammary gland that may contribute to tumor progression.

cancer biology↗

Age-dependent roles of cardiac remodeling in sepsis defense and pathogenesis

Disease tolerance is a defense strategy essential for survival of infections, limiting physiological damage without killing the pathogen. The disease course and pathology a pathogen may cause can change over the lifespan of a host due to the structural and functional physiological changes that accumulate with age. Since successful disease tolerance responses require the host to engage mechanisms that are compatible with the disease course and pathology caused by an infection, we predicted that this defense strategy would change with age. Animals infected with a lethal dose 50 (LD50) of a pathogen often display distinct health and sickness trajectories due to differences in disease tolerance, and thus can be used to delineate tolerance mechanisms. Using a polymicrobial sepsis model, we found that despite having the same LD50, old and young susceptible mice exhibited distinct disease courses. Young survivors employed a cardioprotective mechanism via FoxO1-mediated regulation of the ubiquitin-proteosome system that was necessary for survival and protection from cardiomegaly. This same mechanism was a driver of sepsis pathogenesis in aged hosts, causing catabolic remodeling of the heart and death. Our findings have implications for the tailoring of therapy to the age of an infected individual and suggest that disease tolerance alleles may exhibit antagonistic pleiotropy.

immunology↗

Genomic insertion locus and Cas9 expression in the germline affect CRISPR/Cas9-based gene drive performance in the yellow fever mosquito Aedes aegypti

The yellow fever mosquito Aedes aegypti is a major vector of arthropod-borne viruses, including dengue, chikungunya, and Zika. A novel approach to mitigate arboviral infections is to generate mosquitoes refractory to infection by overexpressing antiviral effector molecules. Such an approach requires a mechanism to spread these antiviral effectors through a population, for example, by using CRISPR/Cas9-based gene drive (GD) systems. Critical to the design of a single-locus autonomous GD is that the selected genomic locus be amenable to both GD and appropriate expression of the antiviral effector. In our study, we used reverse engineering to target two intergenic genomic loci, which had previously shown to be highly permissive for antiviral effector gene expression, and we further investigated the use of three promoters (nanos, {beta}2-tubulin, or zpg) for Cas9 expression. We then quantified the accrual of insertions or deletions (indels) after single generation crossings, measured maternal effects, and assessed fitness costs associated with the various transgenic lines to model the rate of GD fixation. Overall, MGDrivE modeling suggested that when an autonomous GD is placed into an intergenic locus, the GD system will eventually be blocked by the accrual of GD blocking resistance alleles and ultimately be lost in the population. Moreover, while genomic locus and promoter selection were critically important for the initial establishment of the autonomous GD, it was the fitness of the GD line that most strongly influenced the persistence of the GD in the simulated population. As such, we propose that when autonomous CRISPR/Cas9 based GD systems are anchored in an intergenic locus, they temporarily result in a strong population replacement effect, but as GD-blocking indels accrue, the GD becomes exhausted due to the fixation of CRISPR resistance alleles. Significance statementFor the purpose of population replacement, CRISPR/Cas9 based gene drives (GD) have been developed in Anopheles spp. and split GDs have been developed in Ae. aegypti. In our study, we developed autonomous GD in Ae. aegypti and positioned the drives in intergenic loci ideal for the expression of antiviral effector genes. Our results suggest that when the GD is placed into an intergenic locus, there is rapid introgression of the GD resulting in a transient population replacement followed by loss of the drive as resistance alleles accrue. Fitness of the transgenic lines and maternal deposition of CRISPR/Cas9 components were the major contributing factors affecting the perseverance of the GD in our population models.

synthetic biology↗

Paratransgenic manipulation of tsetse miR275 alters the physiological homeostasis of the flys midgut environment

Tsetse flies are vectors of parasitic African trypanosomes (Trypanosoma spp.). Current disease control methods include fly-repelling pesticides, trapping flies, and chemotherapeutic treatment of infected people. Inhibiting tsetses ability to transmit trypanosomes by strengthening the flys natural barriers can serve as an alternative approach to reduce disease. The peritrophic matrix (PM) is a chitinous and proteinaceous barrier that lines tsetses midgut. It protects the epithelial cells from the gut lumen content such as food and invading trypanosomes, which have to overcome this physical barrier to establish an infection. Bloodstream form trypanosomes shed variant surface glycoproteins (VSG) into tsetses gut lumen early during the infection establishment. The VSG molecules are internalized by the flys PM-producing cardia, which results in a reduction in tsetse miR275 expression and a sequential molecular cascade that compromises the PM integrity. In the present study, we investigated the role(s) of miR275 in tsetses midgut physiology and trypanosome infection processes by developing a paratransgenic expression system. We used tsetses facultative bacterial endosymbiont Sodalis glossinidius to express tandem antagomir-275 repeats (or miR275 sponge) that constitutively reduce miR275 transcript abundance. This paratransgenic system successfully knocked down miR275 levels in the flys midgut, which consequently obstructed blood digestion and modulated infection outcomes with an entomopathogenic bacteria and with trypanosomes. RNA sequencing of cardia and midgut tissues from the paratransgenic tsetse confirmed that miR275 regulates processes related to the expression of PM-associated proteins and digestive enzymes as well as genes that encode abundant secretory proteins. Our study demonstrates that paratransgenesis can be employed to study microRNA-regulated pathways in arthropods housing symbiotic bacteria. Author SummaryTsetse flies transmit African trypanosomes, which are the parasites that cause sleeping sickness in human in sub-Saharan Africa. When tsetse ingests a blood meal containing trypanosomes, the expression level of a microRNA (miR275) decreases in the flys gut. This process results in a series of events that interrupt the physiological homeostasis of the gut environment. To further understand the function of miR275 in tsetse fly, we genetically modified a tsetses native bacterial symbiont, reintroduced the genetically modified bacterium back into the fly, and successfully knocked down the miR275 expression in tsetses midgut. These paratransgenic flies (which house genetically modified bacteria) presented impaired digestive processes and were highly susceptible to infection with trypanosomes. Lastly, we discovered that miR275 regulates tsetse secretory pathways. Our novel paratransgenic expression system can be applied to study the function of other microRNAs and how they regulate disease transmission in tsetse and other insect systems.

microbiology↗

β-importins Tnpo-SR and Cadmus and the small GTPase Ran promote ovarian cyst formation in Drosophila

Germ cells undergo mitotic expansion via incomplete cytokinesis, forming cysts of undifferentiated cells that remain interconnected prior to meiotic initiation, through mechanisms that are not well-defined. In somatic cells, Ras-related nuclear protein (Ran) spatiotemporally regulates mitotic spindle assembly, cleavage furrow formation and abscission. Here, we identify Ran and {beta}-importins as critical regulators of cyst development in the Drosophila ovary. Depletion of Ran or the {beta}-importins Tnpo-SR and cadmus disrupts oocyte selection and results in egg chambers with variable numbers of germ cells, suggesting abnormal cyst development and cyst fragmentation. We demonstrate that Ran, Tnpo-SR, and Cadmus regulate key cellular processes during cyst formation, including cell cycle dynamics, fusome biogenesis, and ring canal stability, yet do so independently of mitotic spindle assembly. Further, Tnpo-SR and Cadmus control cyclin accumulation and suppress cytokinesis independent of Ran-GTP, suggesting that {beta}-importins sequester protein cargos that normally promote the mitotic-to-meiotic transition. Our data demonstrates that Ran and {beta}-importins are critical for germ cell cyst formation, a role that is likely conserved in other organisms. SUMMARY STATEMENTRan and two {beta}-importins function coordinately to promote oocyte selection and cyst development in the Drosophila ovary.

developmental biology↗

Obesity-Activated Lung Stomal Cells Promote Myeloid-Lineage Cell Accumulation and Breast Cancer Metastasis

Obesity is correlated with increased incidence of breast cancer metastasis, however the mechanisms underlying how obesity promotes metastasis are unclear. In a diet-induced obesity mouse model, obesity enhanced lung metastases in both the presence and absence of primary mammary tumors and increased recruitment of myeloid lineage cells into the lungs. In the absence of tumors, obese mice demonstrated increased numbers of myeloid lineage cells and elevated collagen fibers within the lung stroma, reminiscent of pre-metastatic niches formed by primary tumors. Lung stromal cells isolated from obese non-tumor-bearing mice showed increased proliferation, contractility, and expression of extracellular matrix, inflammatory markers, and TGF{beta}1. Conditioned media from lung stromal cells from obese mice promoted myeloid lineage cell migration in vitro in response to CSF2 expression and enhanced invasion of tumor cells. Together, these results suggest that prior to tumor formation, obesity alters the lung microenvironment, creating niches conducive for metastatic growth.

cancer biology↗

Astroglia in lateral habenula is essential for antidepressant efficacy of light

Successful antidepressant (AD) treatments are still difficult to achieve. Recently, bright light stimulation (BLS) was shown effective in non-seasonal depression but its mode of action remains elusive. We demonstrate here, using a new mouse model of depression resistant to ADs including ketamine, that chemogenetic activation of lateral habenula (LHb) astroglia prevented the potentiating effect of BLS on the AD response. Additionally, the beneficial action of BLS was associated with upregulation of a specific part of the prefrontal cortex opioid system. These results show that improved behavioral outcome produced by BLS requires habenular astroglia and endogenous opioids as crucial buffer systems.

neuroscience↗

Genetic characterization of outbred Sprague Dawley rats and utility for genome-wide association studies

Sprague Dawley (SD) rats are among the most widely used outbred laboratory rat populations. Despite this, the genetic characteristics of SD rats have not been clearly described, and SD rats are rarely used for experiments aimed at exploring genotype-phenotype relationships. In order to use SD rats to perform a genome-wide association study (GWAS), we collected behavioral data from 4,625 SD rats that were predominantly obtained from two commercial vendors, Charles River Laboratories and Harlan Sprague Dawley Inc. Using double-digest genotyping-by-sequencing (ddGBS), we obtained dense, high-quality genotypes at 291,438 SNPs across 4,061 rats. This genetic data allowed us to characterize the variation present in Charles River vs. Harlan SD rats. We found that the two populations are highly diverged (FST > 0.4). Furthermore, even for rats obtained from the same vendor, there was strong population structure across breeding facilities and even between rooms at the same facility. We performed multiple separate GWAS by fitting a linear mixed model that accounted population structure and using meta-analysis to jointly analyze all cohorts. Our study examined Pavlovian conditioned approach (PavCA) behavior, which assesses the propensity for rats to attribute incentive salience to reward-associated cues. We identified 46 significant associations for the various metrics used to define PavCA. The surprising degree of population structure among SD rats from different sources has important implications for their use in both genetic and non-genetic studies. Author SummaryOutbred Sprague Dawley rats are among the most commonly used rats for neuroscience, physiology and pharmacological research; in the year 2020, 4,188 publications contained the keyword "Sprague Dawley". Rats identified as "Sprague Dawley" are sold by several commercial vendors, including Charles River Laboratories and Harlan Sprague Dawley Inc. (now Envigo). Despite their widespread use, little is known about the genetic diversity of SD. We genotyped more than 4,000 SD rats, which we used for a genome-wide association study (GWAS) and to characterize genetic differences between SD rats from Charles River Laboratories and Harlan. Our analysis revealed extensive population structure both between and within vendors. The GWAS for Pavlovian conditioned approach (PavCA) identified a number of genome-wide significant loci for that complex behavioral trait. Our results demonstrate that, despite sharing an identical name, SD rats that are obtained from different vendors are very different. Future studies should carefully define the exact source of SD rats being used and may exploit their genetic diversity for genetic studies of complex traits.

genetics↗