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Bennett, S. N.

Publications and source records attributed to Bennett, S. N..

9 recordsLinked to original sources

Discovery of frameshift-associated TCRs following personalized neoantigen vaccination in a patient with osteosarcoma

Personalized antigen-directed immunotherapies, including personalized cancer vaccines, are emerging as promising therapeutic modalities for a range of cancer types. Immune monitoring can be used to evaluate the efficacy of a vaccine in stimulating the immune response pre- and post-vaccination; however, such approaches typically stop short of identifying which T cell receptors (TCRs) are functionally driving therapeutic responses. Here, we present a case report of immune monitoring and subsequent TCR discovery experiments following administration of personalized cancer vaccines in a patient with locally recurrent osteosarcoma. Whole PBMCs were stimulated with vaccine peptides (>16 AA) in vitro for 11 days, after which IFN{gamma} ELISPOT identified total T cell responses for 12 of 15 tested peptides post-vaccination. In vitro expanded samples were submitted for 10x single-cell TCR sequencing, from which 26 TCRs were chosen for generation of TCR-T cells based on clonal expansion and culture specificity. Of the generated TCR-T cells, 25 produced functional TCRs, 4 of which were specific to vaccine peptides. However, downstream testing revealed each was MHC class-II restricted. To address this, we repeated the in vitro stimulations with co-cultures of isolated CD8+ T cells with autologous dendritic cells, and cultures of whole PBMCs with anti-MHC class-II blocking antibody. These cultures yielded 10 additional TCRs, 2 of which were responsive to a vaccine peptide containing a MAP2 frameshift mutation. These findings demonstrate an effective approach for leveraging post-vaccination expanded antigen-specific T cell populations for discovery of novel T cell receptors for downstream cellular therapies.

immunology↗

Aberrant oxidative metabolism selects for TET2-deficient hematopoietic stem and progenitor cells

The mechanism(s) driving selective expansion of mutant hematopoietic stem and progenitor cells (HSPC) in clonal hematopoiesis (CH) are incompletely understood. Here, we address the role of metabolism in selection for HSPC with loss of function mutations in TET2. Loss of Tet2 in murine HSPC triggers overexpression of glycolysis and oxidative phosphorylation genes and increased oxidative metabolism via an enlarged mitochondrial network. However, Tet2-deficient HSPC maintain a normal redox state. Strikingly, compound loss of the rate-limiting pentose phosphate pathway (PPP) enzyme glucose-6-phosphate dehydrogenase (G6PD) triggers increased reactive oxygen species and impairs the fitness of Tet2-deficient HSPC. We find that aberrant oxidative metabolism is also a feature of HSPC in human CH and clonal cytopenia of unknown significance (CCUS). Overall, our data point to aberrant metabolism as a critical and conserved driver of selection in TET2-deficient CH and identify the PPP as a crucial compensatory pathway needed to maintain their selective advantage. Statement of SignificanceThis study identifies oxidative metabolism as a critical driver of selection for TET2-deficient HSPC in clonal hematopoiesis (CH). It also demonstrates that cellular redox state is a vulnerability that impairs their fitness. These insights establish targetable metabolic pathway(s) that could be exploited in the setting of TET2 mutant CH.

cancer biology↗

Data-driven analysis identifies female-specific social modulation deficit after chronic social defeat stress

BackgroundChronic social defeat stress is a widely used depression model in male mice. Several proposed adaptations extend this model to females with variable, often marginal effects. We examine the if widely used male-defined metrics of stress are suboptimal in females and reveal sex-specific adaptations. MethodsUsing a data-driven method we comprehensively classified social interaction behavior in 761 male and female mice after chronic social witness/defeat stress, examining social modulation of behavioral frequencies and associations with conventional metrics (i.e., social interaction (SI) ratio). ResultsSocial stress induces distinct behavioral adaptation patterns in males and females. SI ratio leads to underpowered analyses in females with limited utility to differentiate susceptibility/resilience. Data-driven analyses reveal failure of social adaptation in stressed female mice that is captured in attenuated velocity change from no target to target tests ({Delta}Velocity) and validate this in three female social stress models. Combining SI ratio and {Delta}Velocity optimally differentiates susceptibility/ resilience in females and this metric reveals resilient-specific adaptation in a resilience-associated neural circuit in female mice. ConclusionsWe demonstrate that psychological or physical social defeat stress induces similar deficits in females that is qualitatively distinct from male deficits and inadequately sampled by male-defined metrics. We identify modulation of locomotion as a robust and easily implementable metric for rigorous research in female mice. Overall, our findings highlight the need to critically evaluate sex differences in behavior and implement sex-based considerations in preclinical model design.

neuroscience↗

Early-life stress alters postnatal chromatin development in the nucleus accumbens

Early-life stress (ELS) sensitizes individuals to subsequent stressors to increase lifetime risk for psychiatric disorders. Within the nucleus accumbens (NAc) -- a key limbic and reward-associated brain region -- ELS sensitizes both cellular and transcriptional response to later stress, which are programmed by enduring epigenetic changes. Among the histone modifications persistently enriched by ELS in NAc is H3K4me1, which is associated with open chromatin and epigenetic priming of genomic enhancers. Here, we sought to determine whether H3K4me1 enrichment in NAc was sufficient to prime cellular and behavioral responses to adult stress. Viral-mediated overexpression of the histone H3 monomethyltransferase Setd7 in juvenile NAc induced lifelong chromatin changes and predominately opened chromatin at long-range cis-regulatory elements predicted to enhance immediate early-genes and transcriptional regulators of mesolimbic development and synaptic activity. These epigenetic changes altered physiological properties of D2-type medium spiny neurons in NAc to resemble neurons of stressed mice, without significantly altering D1-type neurons. Finally, juvenile -- but not adult -- Setd7 overexpression and H3K4me1 enrichment in NAc enhanced behavioral sensitivity to future stress. Together, these data indicate that altered postnatal chromatin development in NAc by H3K4me1 enrichment is sufficient to prime lifelong transcriptional, physiological, and behavioral stress sensitivity.

neuroscience↗

Early-life stress alters chromatin modifications in VTA to prime stress sensitivity

Early-life stress increases sensitivity to subsequent stress, which has been observed at behavioral, neural activity, and gene expression levels. However, the molecular mechanisms underlying such long-lasting sensitivity are poorly understood. We tested the hypothesis that persistent changes in transcription and transcriptional potential were maintained at the level of the epigenome, through changes in chromatin. We used a combination of bottom-up mass spectrometry, viral-mediated epigenome-editing, RNA-sequencing, patch clamp electrophysiology of dopamine neurons, and behavioral quantification in a mouse model of early-life stress, focusing on the ventral tegmental area (VTA), a dopaminergic brain region critically implicated in motivation, reward learning, stress response, and mood and drug disorders. We found that early-life stress alters histone dynamics in VTA, including enrichment of histone-3 lysine-4 monomethylation -- associated with open chromatin and primed or active enhancers -- and the H3K4 monomethylase Setd7. Mimicking early-life stress through postnatal overexpression of Setd7 and enrichment of H3K4me1 in VTA sensitizes transcriptional, physiological, and behavioral response to adult stress. These findings link early-life stress experience to long-term stress hypersensitivity within the brains dopaminergic circuitry, providing a mechanism by which early-life stress increases risk for mood and anxiety disorders later in life.

neuroscience↗

Thyroid hormones mediate the impact of early-life stress on ventral tegmental area gene expression and behavior

Proper thyroid function is essential to the developing brain, including dopamine neuron differentiation, growth, and maintenance. Stress across the lifespan impacts thyroid hormone signaling and anxiety disorders and depression have been associated with thyroid dysfunction (both hypo- and hyper-active). However, less is known about how stress during postnatal development impacts thyroid function and related brain development. Our previous work in mice demonstrated that early-life stress (ELS) transiently impinged on expression of a transcription factor in dopamine neurons shown to be regulated by thyroid hormones. We hypothesized that thyroid hormone signaling may link experience of ELS with transcriptional dysregulation within the dopaminergic midbrain, and ultimately behavior. Here, we find that ELS transiently increases thyroid-stimulating hormone levels (inversely related to thyroid signaling) in both male and female mice at P21, an effect which recovers by adolescence. We next tested whether transient treatment of ELS mice with synthetic thyroid hormone (levothyroxine, LT4) could ameliorate the impact of ELS on sensitivity to future stress, and on expression of genes related to dopamine neuron development and maintenance, thyroid signaling, and plasticity within the ventral tegmental area. Among male mice, but not females, juvenile LT4 treatment prevented hypersensitivity to adult stress. We also found that rescuing developmental deficits in thyroid hormone signaling after ELS restored levels of some genes altered directly by ELS, and prevented alterations in expression of other genes sensitive to the second hit of adult stress. These findings suggest that thyroid signaling mediates the deleterious impact of ELS on VTA development, and that temporary treatment of hypothyroidism after ELS may be sufficient to prevent future stress hypersensitivity.

neuroscience↗

A SMART method for efficiently isolating monoclonal antibodies from individual rhesus macaque memory B cells

Characterizing antigen-specific B cells is a critical component of vaccine and infectious disease studies in rhesus macaques (RMs). However, it is challenging to capture immunoglobulin variable (IgV) genes from individual RM B cells using 5 multiplex (MTPX) primers in nested PCR reactions. In particular, the diversity within RM IgV gene leader sequences necessitates the use of large 5 MTPX primer sets to amplify IgV genes, decreasing PCR efficiency. To address this problem, we developed a switching mechanism at the 5 ends of the RNA transcript (SMART)-based method for amplifying IgV genes from single RM B cells, providing unbiased capture of Ig heavy and light chain pairs for cloning antibodies. We demonstrate this technique by isolating simian immunodeficiency virus (SIV) envelope-specific antibodies from single-sorted RM memory B cells. This approach has several advantages over existing methods for PCR cloning antibodies from RMs. First, optimized PCR conditions and SMART 5 and 3 rapid amplification of cDNA ends (RACE) reactions generate full-length cDNAs from individual B cells. Second, it appends synthetic primer binding sites to the 5 and 3 ends of cDNA during synthesis, allowing for PCR amplification of low-abundance antibody templates. Third, universal 5 primers are employed to amplify the IgV genes from cDNA, simplifying the primer mixes in the nested PCR reactions and improving the recovery of matched heavy and light chain pairs. We anticipate this method will enhance the isolation of antibodies from individual RM B cells, supporting the genetic and functional characterization of antigen-specific B cells.

immunology↗

Reactivation of early-life stress-sensitive neuronal ensembles contributes to lifelong stress hypersensitivity

Early-life stress (ELS) is one of the strongest lifetime risk factors for depression, anxiety, suicide, and other psychiatric disorders, particularly after facing additional stressful events later in life. Human and animal studies demonstrate that ELS sensitizes individuals to subsequent stress. However, the neurobiological basis of such stress sensitization remains largely unexplored. We hypothesized that ELS-induced stress sensitization would be detectable at the level of neuronal ensembles, such that cells activated by ELS would be more reactive to adult stress. To test this, we leveraged transgenic mice to genetically tag, track, and manipulate experience-activated neurons. We found that in both male and female mice, ELS-activated neurons within the nucleus accumbens (NAc), and to a lesser-extent the medial prefrontal cortex, were preferentially reactivated by adult stress. To test whether reactivation of ELS-activated ensembles in the NAc contributes to stress hypersensitivity, we expressed hM4Dis receptor in control or ELS-activated neurons of pups and chemogenetically inhibited their activity during experience of adult stress. Inhibition of ELS-activated NAc neurons, but not control-tagged neurons, ameliorated social avoidance behavior following chronic social defeat stress in males. These data provide evidence that ELS-induced stress hypersensitivity is encoded at the level of corticolimbic neuronal ensembles.

neuroscience↗

A comparison of asymmetric before-after control impact (aBACI) and staircase experimental designs for testing the effectiveness of stream restoration

Before-after-control-impact (BACI) experimental designs are commonly used in large-scale experiments to test for environmental impacts. However, high natural variability of environmental conditions and populations, and low replication in both treatment and control areas in time and space hampers detection of responses. We compare the power of two asymmetric BACI (aBACI) designs to two staircase designs for detecting changes in juvenile steelhead (Oncorhynchus mykiss) abundance associated with a watershed-scale stream restoration experiment. We performed a simulation study to estimate the effect of a 25% increase in steelhead abundance using spatial and temporal estimates of variance from an ongoing study, and determined the power of each design. Experimental designs were then applied to three streams and each stream was composed of three 4 km long sections. We compared the power of a single treatment section in one stream (BACI-1), three simultaneous treatments of all sections in one stream (BACI-3), three sequential treatments in one stream (STAIRCASE-1), and three sequential treatments in one section in each stream (STAIRCASE-3). All designs had [≥] 94% power to detect a 25% increase in abundance assuming average variance. Under worst-case variance (i.e., upper 95% confidence limits of historical variance estimates), the STAIRCASE-3 design outperformed the BACI-1, BACI-3, and STAIRCASE-1 designs (i.e., 77%, 41%, 8%, and 33% power respectively). All the designs estimated the effect of the simulated 25% abundance increase, but the length of the confidence interval was much shorter for the STAIRCASE-3 design compared to the other designs, which had confidence intervals 58-596% longer. The STAIRCASE-3 design continued to have high power (88%) to detect a 10% change in abundance, but the power of the other designs was much lower (range 34-56%). Our study demonstrates that staircase designs can have significant advantages over BACI designs and therefore should be more widely used for testing environmental impacts.

scientific communication and education↗