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Goodyear, L. J.

Publications and source records attributed to Goodyear, L. J..

11 recordsLinked to original sources

Multi-omic responses to acute exercise in abdominal subcutaneous adipose tissue of sedentary adults: findings from MoTrPAC

Exercise induces widespread health benefits across multiple tissues, yet the acute molecular responses in human adipose tissue remain poorly defined. The Molecular Transducers of Physical Activity Consortium (MoTrPAC) profiled temporal molecular changes in abdominal subcutaneous adipose tissue (ASAT) following a single bout of exercise. Healthy sedentary adults were randomized to endurance (EE), resistance (RE), or control (CON) groups. ASAT biopsies were collected pre-exercise and at 45min, 4hr, and 24hr post-exercise, followed by transcriptomic, proteomic, phosphoproteomic, and metabolomic analyses. EE and RE elicited distinct, time-resolved molecular programs involving angiogenesis, extracellular matrix remodeling, mitochondrial metabolism, substrate utilization, and circadian regulation. Phosphoproteomics revealed acute changes in cytoskeletal and branched-chain amino acid metabolism proteins associated with glycemic control. Temporal metabolomic shifts were cell-type-specific. Finally, we identified candidate adipose-derived exerkines with predicted endocrine actions. This multi-omic map of acute ASAT responses offers insight into adipose-specific mechanisms by which exercise promotes metabolic health.

systems biology↗

Rejuvenation of white adipose tissue in a longitudinal heterochronic transplantation model

Exposure to a younger system can induce organismal rejuvenation, yet whether all tissues can be rejuvenated and by what mechanisms remains understudied. We performed heterochronic and isochronic transplantation of subcutaneous white adipose tissue (WAT) between young and old mice and longitudinally tracked changes in biological age. Transplantation accelerated tissue aging, and the molecular age of grafts shifted toward that of the host. Most importantly, old WAT was rejuvenated in a young body. Epigenetic and transcriptomic clocks revealed a reduction of predicted age, accompanied by coordinated activation of canonical and previously unrecognized thermogenic pathways. Molecular rejuvenation was further supported by architectural changes toward a youthful state, including reduced lipid droplet size and decreased cellular heterogeneity. Mitochondrial abundance and morphology remained unchanged, while collagen deposition increased. These results demonstrate that WAT biological age is partially reversible and identify molecular and cellular features underlying its rejuvenation

systems biology↗

Type 2 Diabetes and Obesity Alter Exercise Training-Induced Transcriptional Adaptations to Subcutaneous White Adipose Tissue

White adipose tissue (WAT) dysfunction contributes to obesity-associated metabolic disease and type 2 diabetes (T2D). Rodent studies have demonstrated that exercise training improves WAT function, but molecular studies investigating exercise training effects on WAT in humans have been limited, particularly in the context of metabolic disease. Here, we defined the subcutaneous WAT (scWAT) transcriptome in middle-aged adults (10 male, 19 female) that were classified by lower BMI (<27 kg/m2), higher BMI ([&ge;]27 kg/m2), and T2D status before and after a 10-week endurance exercise regimen. At baseline, 624 genes were significantly upregulated and 112 genes downregulated in the scWAT from higher BMI participants compared to lower BMI. There was a spectrum of pathway dysregulation in scWAT in higher BMI individuals, ranging from increased markers of extracellular matrix (ECM) deposition and inflammation to decreased circadian rhythm gene expression. In people with T2D, there were additional transcriptomic differences such as translation-related pathways, selenoamino acid metabolism, and proteoglycans. Exercise training had robust effects on the transcriptome regardless of metabolic status, and notably, for the high BMI and T2D groups, training reversed several of the detrimental gene expression patterns in a cell-type-specific manner. These beneficial exercise-induced transcriptomic adaptations significantly correlated with lower levels of free fatty acids and blood pressure, particularly in participants with higher BMI and T2D. By integrating our exercise training-modulated genes with GWAS meta-analysis of physical activity, genes influenced by exercise training in the higher BMI group showed a significant enrichment in genetic associations of exercise traits in the population. A circadian rhythm-related transcription factor NR1D1 was enriched in enhancers linked with both the exercise differentially expressed genes (DEGs) and GWAS signals, suggesting a link between the circadian rhythm and training-induced adaptations. These findings demonstrate that obesity and T2D result in marked, progressive alterations in cell-type specific gene transcription in scWAT, while endurance exercise training reverses many of the metabolic disease-associated adaptations. Identification of novel molecular pathways regulated by exercise training can lead to therapeutic targets for obesity and metabolic disease.

molecular biology↗

Exercise training remodels inter-organ endocrine networks

Exercise induces organism-wide molecular adaptations, partly mediated by humoral factors released in response to acute and chronic physical activity. However, the extent and specificity of endocrine effects from training-induced secreted factors remain unclear. Here, we applied systems genetics approaches to quantify inter-organ endocrine networks using multi-tissue transcriptomics and proteomics data collected from endurance-trained rats in The Molecular Transducers of Physical Activity Consortium (MoTrPAC). Eight weeks of endurance training significantly altered both the magnitude and specificity of endocrine effects across multiple origin-target tissue pairs. Subcutaneous white adipose tissue emerged as a key endocrine regulator impacted by training, while extracellular matrix-derived factors were identified as globally regulated secretory features in trained vs sedentary animals. Notably, secretory Wnt signaling factors were identified as key mediators of exercise-induced endocrine adaptations in multiple tissues. Our systems genetics framework provides an unprecedented atlas of inter-organ communication significantly remodeled by endurance exercise, serving as a valuable resource for novel exerkine discovery.

physiology↗

Effects of maternal exercise modes on infant cord blood proteome

The aim of this study was to show the effects of different maternal exercise modes on infant cord blood proteome. We used infant cord blood from two randomized controlled trials where women with a wide range of BMI and free of pregnancy complications participated in controlled and supervised aerobic, resistance, or combination (aerobic+resistance) exercise from <16 weeks of gestation until delivery. Results of this study showed that infant cord blood proteome is altered in a maternal exercise mode specific manner. Additionally, results showed 61 downregulated proteins common to all exercise modes, which correspond to gas transport, cellular stress response, reactive oxygen species metabolism, and other biological processes. Collectively, these data demonstrate the differential effect of maternal exercise modes on infant cord blood proteome.

physiology↗

Maternal exercise alters placental proteome in an exercise mode-specific manner

Maternal exercise is a widely recommended and safe intervention associated with the improvement of maternal gestational and infant metabolic health. While various modes of exercise are deemed safe during pregnancy, the effects of supervised maternal aerobic, resistance, and combination (aerobic+resistance) exercise remain understudied. Specifically, it remains unknown how different modes of maternal exercise affect the placenta, an organ central to maternal-fetal communication and successful pregnancy outcomes. This study aimed to characterize the placental proteomic changes in response to controlled and supervised maternal exercise during gestation. Results showed that the placental proteomic landscape changes in an maternal exercise mode-specific way. Additionally, proteomics revealed that [~]20% of the identified placental proteins were associated with maternal exercise volume during gestation. These results highlight the differential effect maternal exercise modes have on the placental proteome and further implicate the placenta in mediating the effects of maternal exercise on maternal and infant health.

developmental biology↗

Exercise Training and Cold Exposure Trigger Distinct Molecular Adaptations to Inguinal White Adipose Tissue

Exercise training and cold exposure both improve systemic metabolism, but the mechanisms are not well-established. We tested the hypothesis that adaptations to inguinal white adipose tissue (iWAT) are critical for these beneficial effects by determining the impact of exercise-trained and cold-exposed iWAT on systemic glucose metabolism and the iWAT proteome and secretome. Transplanting trained iWAT into sedentary mice improved glucose tolerance, while cold-exposed iWAT transplantation showed no such benefit. Compared to training, cold led to more pronounced alterations in the iWAT proteome and secretome, downregulating >2,000 proteins but also boosting iWATs thermogenic capacity. In contrast, only training increased extracellular space and vesicle transport proteins, and only training upregulated proteins that correlate with favorable fasting glucose, suggesting fundamental changes in trained iWAT that mediate tissue-to-tissue communication. This study defines the unique exercise training- and cold exposure-induced iWAT proteomes, revealing distinct mechanisms for the beneficial effects of these interventions on metabolic health. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=197 SRC="FIGDIR/small/562635v1_ufig1.gif" ALT="Figure 1"> View larger version (100K): org.highwire.dtl.DTLVardef@1ee3ffaorg.highwire.dtl.DTLVardef@aa3f48org.highwire.dtl.DTLVardef@120a8edorg.highwire.dtl.DTLVardef@1329dbb_HPS_FORMAT_FIGEXP M_FIG C_FIG

physiology↗

Sexual dimorphism and the multi-omic response to exercise training in rat subcutaneous white adipose tissue

Subcutaneous white adipose tissue (scWAT) is a dynamic storage and secretory organ that regulates systemic homeostasis, yet the impact of endurance exercise training and sex on its molecular landscape has not been fully established. Utilizing an integrative multi-omics approach with data generated by the Molecular Transducers of Physical Activity Consortium (MoTrPAC), we identified profound sexual dimorphism in the dynamic response of rat scWAT to endurance exercise training. Despite similar cardiorespiratory improvements, only male rats reduced whole-body adiposity, scWAT adipocyte size, and total scWAT triglyceride abundance with training. Multi-omic analyses of adipose tissue integrated with phenotypic measures identified sex-specific training responses including enrichment of mTOR signaling in females, while males displayed enhanced mitochondrial ribosome biogenesis and oxidative metabolism. Overall, this study reinforces our understanding that sex impacts scWAT biology and provides a rich resource to interrogate responses of scWAT to endurance training.

molecular biology↗

Temporal dynamics of the multi-omic response to endurance exercise training across tissues

Regular exercise promotes whole-body health and prevents disease, yet the underlying molecular mechanisms throughout a whole organism are incompletely understood. Here, the Molecular Transducers of Physical Activity Consortium (MoTrPAC) profiled the temporal transcriptome, proteome, metabolome, lipidome, phosphoproteome, acetylproteome, ubiquitylproteome, epigenome, and immunome in whole blood, plasma, and 18 solid tissues in Rattus norvegicus over 8 weeks of endurance exercise training. The resulting data compendium encompasses 9466 assays across 19 tissues, 25 molecular platforms, and 4 training time points in young adult male and female rats. We identified thousands of shared and tissue- and sex-specific molecular alterations. Temporal multi-omic and multi-tissue analyses demonstrated distinct patterns of tissue remodeling, with widespread regulation of immune, metabolism, heat shock stress response, and mitochondrial pathways. These patterns provide biological insights into the adaptive responses to endurance training over time. For example, exercise training induced heart remodeling via altered activity of the Mef2 family of transcription factors and tyrosine kinases. Translational analyses revealed changes that are consistent with human endurance training data and negatively correlated with disease, including increased phospholipids and decreased triacylglycerols in the liver. Sex differences in training adaptation were widespread, including those in the brain, adrenal gland, lung, and adipose tissue. Integrative analyses generated novel hypotheses of disease relevance, including candidate mechanisms that link training adaptation to non-alcoholic fatty liver disease, inflammatory bowel disease, cardiovascular health, and tissue injury and recovery. The data and analysis results presented in this study will serve as valuable resources for the broader community and are provided in an easily accessible public repository (https://motrpac-data.org/). HighlightsO_LIMulti-tissue resource identifies 35,439 analytes regulated by endurance exercise training at 5% FDR across 211 combinations of tissues and molecular platforms. C_LIO_LIInterpretation of systemic and tissue-specific molecular adaptations produced hypotheses to help describe the health benefits induced by exercise. C_LIO_LIRobust sex-specific responses to endurance exercise training are observed across multiple organs at the molecular level. C_LIO_LIDeep multi-omic profiling of six tissues defines regulatory signals for tissue adaptation to endurance exercise training. C_LIO_LIAll data are available in a public repository, and processed data, analysis results, and code to reproduce major analyses are additionally available in convenient R packages. C_LI

molecular biology↗

Exercise Training Remodels Adipocyte-Specific Extracellular Matrix Proteins and Alters Innervation and Vascularization in Inguinal White Adipose Tissue (iWAT)

Inguinal white adipose tissue (iWAT) is essential for the beneficial effects of exercise training on metabolic health. Extracellular matrix (ECM) composition, innervation, and vascularization are all important regulators of iWAT function, yet whether exercise training improves these structural components of iWAT is unknown. Using biochemical, imaging, and multi-omics analyses we find that 11-days of wheel running in male mice causes profound iWAT remodeling including decreased ECM deposition and increased vascularization and innervation. We identify adipose stem cells as the main contributors to training-induced ECM remodeling, determine that training causes a shift from hypertrophic to insulin-sensitive adipocyte subpopulations, show that the PRDM16 transcriptional complex is necessary for iWAT remodeling and beiging, and discover neuronal growth regulator 1 (NEGR1) as a link between PRDM16 and neuritogenesis. Exercise training leads to remarkable adaptations to iWAT structure and cell-type composition that can confer beneficial changes in tissue metabolism. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=139 SRC="FIGDIR/small/503375v1_ufig1.gif" ALT="Figure 1"> View larger version (42K): org.highwire.dtl.DTLVardef@fd590eorg.highwire.dtl.DTLVardef@e1dd02org.highwire.dtl.DTLVardef@74be24org.highwire.dtl.DTLVardef@6f6e58_HPS_FORMAT_FIGEXP M_FIG C_FIG

physiology↗