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Biology subjects

Ryan, T. E.

Publications and source records attributed to Ryan, T. E..

14 recordsLinked to original sources

Ovariectomy and Chemical Ovarian Failure Exacerbate Atherosclerosis without Impairing Limb Recovery in Experimental Peripheral Artery Disease

BackgroundPeripheral artery disease is a major manifestation of atherosclerotic cardiovascular disease (ASCVD) that affects both men and women. In women, menopause increases the ASCVD risk. However, preclinical ASCVD research has historically been conducted predominantly in males, with relatively few studies focused on females and even fewer incorporating menopause models that more closely reflect human ASCVD pathobiology. Herein, we tested whether the chemical 4-vinylcyclohexene diepoxide (4-VCD)-induced ovarian failure or ovariectomy (OVX) would drive atherosclerotic development and worsen ischemic limb pathophysiology. MethodsFemale C57BL/6J mice were injected with adeno-associated virus-mediated encoding a gain-of-function mutant PCSK9 and fed an atherogenic diet for 23 weeks. Based on the baseline body weight, mice were randomly assigned to normally cycling controls (CON), 4-VCD, or OVX groups. Three weeks after the conformation of ovarian failure (4-VCD) or surgical ovarian removal (OVX), hindlimb ischemia (HLI) was induced via femoral artery ligation, and limb perfusion recovery and limb muscle performance were assessed. ResultsBoth 4-VCD treatment and OVX reduced uterus mass, without impacting body weight or composition, or circulating cholesterol levels compared to CON mice. Despite the similar metabolic and cholesterol profiles, atherosclerotic lesion areas were 1.5-1.7-fold greater in 4-VCD and OVX mice than CON mice. Perfusion recovery following HLI and plantar flexor muscle function in the ischemic limb were similar across groups, though muscle oxygenation was reduced in 4-VCD and OVX groups. ConclusionsOvarian failure and removal exacerbated atherosclerotic development but had minimal impacts on perfusion recovery and limb function following HLI. These findings confirm the inclusion of menopausal models, whether through ovarian failure or OVX, should be carefully considered to improve translatability of preclinical ASCVD studies, especially for womens health. Clinical PerspectiveO_ST_ABSWhat is New?C_ST_ABSWe demonstrate that both gradual ovarian failure (4-VCD) and surgical ovariectomy exacerbate atherosclerotic plaque development in a clinically relevant AAV-PCSK9 model, despite similar circulating lipid levels. In contrast, loss of ovarian function did not impair limb perfusion recovery or muscle functional outcomes following hindlimb ischemia, revealing a dissociation between atherosclerotic burden and limb functional recovery in experimental peripheral artery disease (PAD). What are the Clinical Implications?These findings provide new insight into why menopause increases atherosclerotic cardiovascular disease (ASCVD) risk while not necessarily demonstrating proportional impairments in limb recovery following ischemia. The data suggest that menopause-associated factors accelerate large-vessel atherosclerosis independent of circulating lipids, highlighting the need for targeted therapies beyond lipid lowering in postmenopausal women. Moreover, the dissociation between plaque burden and ischemic limb function underscores the importance of assessing functional outcomes in PAD independently of vascular imaging. Finally, these findings suggest that the incorporation of menopause-relevant models in preclinical research should be considered within the context of the specific biological endpoints and translational goals being evaluated.

physiology↗

Mitochondrial Permeability Transition in Skeletal Muscle Phenocopies Muscle Alterations seen in Cancer Cachexia and other Wasting Conditions

Skeletal muscle in wasting conditions often exhibits atrophy, mitochondrial respiratory dysfunction, and fragmentation of the acetylcholine receptor (AChR) cluster at the endplate. The accompanying alterations of mitochondrial morphology suggest mitochondria may be involved in muscle pathology in these conditions. To address this gap, we tested an established pathological mechanism in ischemia-reperfusion injury and neurodegeneration but poorly studied in skeletal muscle: mitochondrial permeability transition (mPT). We tested if mPT recapitulated phenotypes common in wasting conditions, whether tumor-conditioned media (TCM) could promote mPT, and compared differentially expressed genes (DEGs) induced by mPT with DEGs observed in a mouse model of pancreatic cancer cachexia. Inducing mPT in mouse skeletal muscle bundles progressively altered mitochondrial cristae morphology, culminating in breach of the outer mitochondrial membrane. Inducing mPT in mouse muscle fibers increased mROS and Caspase 3 activity and caused atrophy. Inducing mPT caused a complex I mitochondrial respiratory impairment, increased lysosome-mitochondrion co-localization, and fragmented the AChR cluster at the muscle endplate. The Ca2+ threshold for mPT, mitochondrial calcein colocalization and mitochondrial membrane potential were reduced by TCM in skeletal muscle or C2C12 myoblasts, respectively. Knockout of the mPT-regulating protein CypD attenuated the reduction in Ca2+ threshold for mPT by TCM. Inhibitors of mPT attenuated atrophy with TCM in C2C12 and human primary myotubes. Finally, there was overlap between the DEGs of mPT and diaphragm muscle in a mouse model of pancreatic cancer cachexia during the muscle wasting phase. We conclude that mPT should be explored as a therapeutic target in muscle wasting disorders.

physiology↗

Intramuscular Adipose Tissue Accumulation is a Key Determinant of Limb Function in Peripheral Artery Disease

BackgroundPeripheral artery disease (PAD) and its severe form, chronic limb-threatening ischemia (CLTI), significantly impair blood flow to the lower extremities, affecting millions of adults globally. Intramuscular adipose tissue (IMAT) and fibrosis accumulation distinguish patients with CLTI from those with mild PAD, suggesting a role in CLTI pathobiology. However, the functional consequences of IMAT in CLTI remain unclear. MethodsWe compared gastrocnemius muscle samples from patients with PAD/CLTI, intermittent claudication, and non-PAD individuals. We analyzed bulk RNA sequencing, proteomic, lipidomic, and single-cell/nucleus RNA sequencing datasets. Additionally, we used murine models of hindlimb ischemia (HLI) with genetic manipulation of Ppar{gamma}, a key adipogenic transcription factor, specifically in fibro-adipogenic progenitor cells (FAPs), the cellular source of IMAT, to modulate IMAT formation and assessed the impact on limb function and pathology. ResultsPatients with CLTI exhibited significantly elevated expression of adipogenic genes and proteins in muscle specimens when compared to non-PAD controls. Murine models showed that increasing IMAT formation significantly worsened ischemic limb muscle strength and work output. In contrast, preventing IMAT formation significantly improved ischemic limb muscle strength and work output. These findings were consistent across both male and female mice, although females had greater tendency to form IMAT compared with male mice. ConclusionsIMAT accumulation is a key determinant of limb function in PAD/CLTI. Our studies demonstrate that targeting IMAT formation could improve limb function in mice with experimental PAD. Together, these findings suggest that developing strategies to limit or reduce IMAT may improve limb function and walking performance in patients with PAD/CLTI, providing a novel therapeutic avenue to address a critical unmet need. CLINICAL PERSPECTIVEO_ST_ABSWhat is new?C_ST_ABSO_LIIntramuscular adipose tissue accumulation (IMAT) distinguishes patients with chronic limb-threatening ischemia from those with milder peripheral artery disease or those without PAD and directly impairs ischemic limb muscle function. C_LIO_LIGenetic gain- and loss-of-function mouse models demonstrate that increasing IMAT worsens, while preventing IMAT formation improves, ischemic limb strength and performance independent of perfusion. C_LIO_LIAdipogenic signatures in human calf muscle negatively correlates with muscle strength and disease severity, identifying IMAT as a functional biomarker and modifiable target in PAD/CLTI. C_LI What are the clinical implications?O_LIIMAT accumulation represents an underappreciated, non-vascular mechanism contributing to leg dysfunction in PAD/CLTI. C_LIO_LITherapies aimed at limiting or reversing IMAT formation may improve leg strength and walking performance in patients with PAD/CLTI, addressing a critical unmet clinical need. C_LIO_LIIdentifying and targeting cellular pathways regulating IMAT formation from fibro-adipogenic progenitors may complement vascular interventions to enhance functional recovery after revascularization. C_LI

physiology↗

Hepatocyte FAM210A deficiency disrupts mitochondrial function and triggers juvenile steatosis with compensatory repair in adulthood

Mitochondrial dynamics are central to maintaining liver metabolic homeostasis, yet the mechanisms that safeguarding mitochondrial integrity during development and metabolic dysfunction remain poorly defined. Here, we identify Family with sequence similarity 210 member A (FAM210A) as a hepatocyte-enriched mitochondrial regulator essential for postnatal liver maturation. Hepatocyte-specific deletion of Fam210a (Fam210aHKO) in mice caused early growth restriction, reduced body and liver mass, and pronounced hepatic steatosis with glycogen depletion. These defects were accompanied by lower postprandial glucose levels in the fasted-refeeding state, impaired oxidative phosphorylation, reduced mtDNA content, and abnormal cristae architecture. Transcriptomic and proteomic profiling revealed broad suppression of fatty acid, sterol, and bile acid metabolism, with concomitant glutathione stress responses. Mechanistically, FAM210A deficiency disrupted the YME1L-OPA1 axis, driving excessive OPA1 cleavage and cristae destabilization. Strikingly, these juvenile defects were transient and resolved by adulthood, underpinned by enhanced hepatocyte proliferation and mitochondrial biogenesis, consistent with a compensatory stress-adaptive response via the activation of ISR signaling. Together, these findings uncover FAM210A as a developmental safeguard of mitochondrial remodeling in hepatocytes and indicate compensatory programs with therapeutic relevance for chronic liver disease.

physiology↗

Intramuscular adipose tissue physically restricts functional muscle recovery

With age and disease, skeletal muscle is progressively lost and replaced by fibrotic scar and intramuscular adipose tissue (IMAT). While strongly correlated, it remains unclear whether IMAT has a functional impact on muscle. In the present study, we evaluated the effects of IMAT during muscle injury by creating a mouse model where the cellular origin of IMAT, fibro/adipogenic progenitors (FAPs), are prevented from differentiating into adipocytes (FATBLOCK model). We found that blocking IMAT after an adipogenic injury allowed muscle to regenerate more efficiently, resulting in enhanced function. Our data explain why acute muscle injuries featuring IMAT infiltration, such as rotator cuff tears and acute denervation injuries, exhibit poor regeneration and lead to a loss in muscle function. It also demonstrates the therapeutic importance of preventing IMAT formation in acute injuries in order to maximize regeneration and minimize loss in muscle mass and function.

developmental biology↗

A 6-minute Limb Function Assessment for Therapeutic Testing in Experimental Peripheral Artery Disease Models

BackgroundThe translation of promising therapies from pre-clinical models of hindlimb ischemia (HLI) to patients with peripheral artery disease (PAD) has been inadequate. While this failure is multifactorial, primary outcome measures in preclinical HLI models and clinical trials involving patients with PAD are not aligned well. For example, laser Doppler perfusion recovery measured under resting conditions is the most used outcome in HLI studies, whereas clinical trials involving patients with PAD primarily assess walking performance. Here, we sought to develop a 6-min limb function test for preclinical HLI models that assess muscular performance and hemodynamics congruently. MethodsWe developed an in situ 6-min limb function test that involves repeated isotonic (shortening) contractions performed against a submaximal load. Continuous measurement of muscle blood flow was performed using laser Doppler flowmetry. Quantification of muscle power, work, and perfusion are obtained across the test. To assess the efficacy of this test, we performed HLI via femoral artery ligation on several mouse strains: C57BL6J, BALBc/J, and MCK-PGC1 (muscle-specific overexpression of PGC1). Additional experiments were performed using an exercise intervention (voluntary wheel running) following HLI. ResultsThe 6-min limb function test was successful at detecting differences in limb function of C57BL6/J and BALBc/J mice subjected to HLI with effect sizes superior to laser Doppler perfusion recovery. C57BL6/J mice randomized to exercise therapy following HLI had smaller decline in muscle power, greater hyperemia, and performed more work across the 6-min limb function test compared to non-exercise controls with HLI. Mice with muscle-specific overexpression of PGC1 had no differences in perfusion recovery in resting conditions, but exhibited greater capillary density, increased muscle mass and absolute force levels, and performed more work across the 6-min limb function test compared to their wildtype littermates without the transgene. ConclusionThese results demonstrate the efficacy of the 6-min limb function test to detect differences in the response to HLI across several interventions including where traditional perfusion recovery, capillary density, and muscle strength measures were unable to detect therapeutic differences.

physiology↗

Activation of the Aryl Hydrocarbon Receptor in Endothelial Cells Impairs Ischemic Angiogenesis in Chronic Kidney Disease

RationaleChronic kidney disease (CKD) is a strong risk factor for peripheral artery disease (PAD) that is associated with worsened clinical outcomes. CKD leads to accumulation of tryptophan metabolites that associate with adverse limb events in PAD and are ligands of the aryl hydrocarbon receptor (AHR) which may regulate ischemic angiogenesis. ObjectivesTo test if endothelial cell-specific deletion of the AHR (AHRecKO) alters ischemic angiogenesis and limb function in mice with CKD subjected to femoral artery ligation. FindingsMale AHRecKO mice with CKD displayed better limb perfusion recovery and enhanced ischemic angiogenesis compared to wildtype mice with CKD. However, the improved limb perfusion did not result in better muscle performance. In contrast to male mice, deletion of the AHR in female mice with CKD had no impact on perfusion recovery or angiogenesis. Using primary endothelial cells from male and female mice, treatment with indoxyl sulfate uncovered sex-dependent differences in AHR activating potential and RNA sequencing revealed wide ranging sex-differences in angiogenic signaling pathways. ConclusionEndothelium-specific deletion of the AHR improved ischemic angiogenesis in male, but not female, mice with CKD. There are sex- dependent differences in Ahr activating potential within endothelial cells that are independent of sex hormones.

physiology↗

Single Nuclei RNA Sequencing of the Gastrocnemius Muscle in Peripheral Artery Disease

BackgroundLower extremity peripheral artery disease (PAD) is a growing epidemic with limited effecOve treatment options. Herein, we provide a single nuclei atlas of PAD limb muscle to facilitate a better understanding of the composition of cells and transcriptional differences that comprise the diseased limb muscle. MethodsWe obtained gastrocnemius muscle specimens from 20 PAD patients and 12 non-PAD controls. Nuclei were isolated and single nuclei RNA sequencing (snRNAseq) was performed. The composition of nuclei was characterized by iteraOve clustering via principal component analysis, differenOal expression analysis, and the use of known marker genes. BioinformaOcs analysis was performed to determine differences in gene expression between PAD and non-PAD nuclei, as well as subsequent analysis of intercellular signaling networks. Additional histological analyses of muscle specimens accompany the snRNAseq atlas. ResultssnRNAseq analysis indicated a fiber type shim with PAD paOents having fewer Type I (slow/oxidaOve) and more Type II (fast/glycolyOc) myonuclei compared to non-PAD, which was confirmed using immunostaining of muscle specimens. Myonuclei from PAD displayed global upregulation of genes involved in stress response, autophagy, hypoxia, and atrophy. Subclustering of myonuclei also idenOfied populations that were unique to PAD muscle characterized by metabolic dysregulation. PAD muscles also displayed unique transcriptional profiles and increased diversity of transcriptomes in muscle stem cells, regeneraOng myonuclei, and fibro-adipogenic progenitor (FAPs) cells. Analysis of intercellular communication networks revealed FAPs as a major signaling hub in PAD muscle, as well as deficiencies in angiogenic and bone morphogeneOc protein signaling which may contribute to poor limb function in PAD. ConclusionsThis reference snRNAseq atlas provides a comprehensive analysis of the cell composition, transcriptional signature, and intercellular communication pathways that are altered in the PAD condition.

genomics↗

Chronic activation of the aryl hydrocarbon receptor in muscle exacerbates ischemic pathology in chronic kidney disease

Chronic kidney disease (CKD) accelerates the development of atherosclerosis, decreases muscle function, and increases the risk of amputation or death in patients with peripheral artery disease (PAD). However, the cellular and physiological mechanisms underlying this pathobiology are ill-defined. Recent work has indicated that tryptophan-derived uremic toxins, many of which are ligands for the aryl hydrocarbon receptor (AHR), are associated with adverse limb outcomes in PAD. We hypothesized that chronic AHR activation, driven by the accumulation of tryptophan-derived uremic metabolites, may mediate the myopathic condition in the presence of CKD and PAD. Both PAD patients with CKD and mice with CKD subjected to femoral artery ligation (FAL) displayed significantly higher mRNA expression of classical AHR-dependent genes (Cyp1a1, Cyp1b1, and Aldh3a1) when compared to either muscle from the PAD condition with normal renal function (P<0.05 for all three genes) or non-ischemic controls. Skeletal-muscle-specific AHR deletion in mice (AHRmKO) significantly improved limb muscle perfusion recovery and arteriogenesis, preserved vasculogenic paracrine signaling from myofibers, increased muscle mass and contractile function, as well as enhanced mitochondrial oxidative phosphorylation and respiratory capacity in an experimental model of PAD/CKD. Moreover, viral-mediated skeletal muscle-specific expression of a constitutively active AHR in mice with normal kidney function exacerbated the ischemic myopathy evidenced by smaller muscle masses, reduced contractile function, histopathology, altered vasculogenic signaling, and lower mitochondrial respiratory function. These findings establish chronic AHR activation in muscle as a pivotal regulator of the ischemic limb pathology in PAD. Further, the totality of the results provide support for testing of clinical interventions that diminish AHR signaling in these conditions.

physiology↗

IGF-1 therapy improves muscle size and function in experimental peripheral arterial disease

CONDENSED ABSTRACTLower extremity peripheral arterial disease (PAD) has continued to increase in prevalence over the past several decades, yet therapeutic development has remained stagnant. Skeletal muscle health and function has been strongly linked to quality of life and medical outcomes in PAD patients. Using a rodent model of PAD, this study demonstrates that treatment of the ischemic limb with adeno-associated virus-mediated expression of insulin-like growth factor 1 (IGF1) significantly increases muscle size and strength, without improving limb hemodynamics. Interestingly, the effect size of IGF1 therapy was larger in female mice compared to their male counterparts, where substantial improvements in muscle specific force and a reduction in the progression of limb necrosis were observed. These findings indicate that clinical trials should carefully examine sex-dependent effects in experimental PAD therapies.

physiology↗

Skeletal muscle Nox4 knockout prevents and Nox2 knockout blunts loss of maximal diaphragm force in mice with heart failure with reduced ejection fraction

Patients with heart failure with reduced ejection fraction (HFrEF) experience diaphragm weakness that contributes to the primary disease symptoms of fatigue, dyspnea, and exercise intolerance. Weakness in the diaphragm is related to excessive production of reactive oxygen species (ROS), but the exact source of ROS remains unknown. NAD(P)H Oxidases (Nox), particularly the Nox2 and 4 isoforms, are important sources of ROS within skeletal muscle that contribute to optimal cell function. There are reports of increased Nox activity in the diaphragm of patients and animal models of HFrEF, implicating these complexes as possible sources of diaphragm dysfunction in HFrEF. To investigate the role of these proteins on diaphragm weakness in HFrEF, we generated inducible skeletal muscle specific knockouts of Nox2 or Nox4 using the Cre-Lox system and assessed diaphragm function in a mouse model of HFrEF induced by myocardial infarction. Diaphragm maximal specific force measured in vitro was depressed by ~20% with HFrEF. Knockout of Nox4 provided full protection against the loss of maximal force (p < 0.01), while the knockout of Nox2 provided partial protection (7% depression, p < 0.01). Mitochondrial respiration measured in permeabilized diaphragm muscle bundles increased with HFrEF or the knockout of Nox4 from skeletal muscle fibers (p < 0.05). Knockout of Nox2 from skeletal myofibers improved survival from 50 to 80% following myocardial infarction (p = 0.026). Our findings show an important role for skeletal muscle NAD(P)H Oxidases contributing to loss of diaphragm maximal force in HFrEF, along with systemic pathophysiological responses following myocardial infarction.

physiology↗

Reversible thiol oxidation increases mitochondrial electron transport complex enzyme activity but not respiration in cardiomyocytes from patients with end-stage heart failure

Cardiomyocyte dysfunction in patients with end-stage heart failure with reduced ejection fraction (HFrEF) stems from mitochondrial dysfunction that contributes to an energetic crisis. Mitochondrial dysfunction reportedly relates to increased markers of oxidative stress, but the impact of reversible thiol oxidation on myocardial mitochondrial function in patients with HFrEF has not been investigated. In the present study, we assessed mitochondrial function in ventricular biopsies from patients with end-stage HFrEF in the presence and absence of the thiol reducing agent dithiothreitol (DTT). Isolated mitochondria exposed to DTT had increased enzyme activity of complexes I (p = 0.009) and III (p = 0.018) of the electron transport system, while complexes II (p = 0.630) or IV (p = 0.926) showed no changes. However, increased enzyme activity did not carry over to measurements of mitochondrial respiration in permeabilized bundles. Oxidative phosphorylation conductance (p = 0.439), maximal respiration (p = 0.312), and ADP sensitivity (p = 0.514) were unchanged by 5 mM DTT treatment. These results indicate that mitochondrial function can be modulated through reversible thiol oxidation, but other components of mitochondrial energy transfer are rate limiting in end-stage HFrEF. Optimal therapies to normalize cardiac mitochondrial respiration in patients with end-stage HFrEF may benefit from interventions to reverse thiol oxidation that limits complex I and III activities.

physiology↗

Chronic Aryl Hydrocarbon Receptor Activity Phenocopies Smoking-induced Skeletal Muscle Impairment

BackgroundCOPD patients exhibit skeletal muscle atrophy, denervation, and reduced mitochondrial oxidative capacity. Whilst chronic tobacco smoke exposure is implicated in COPD muscle impairment, the mechanisms involved are ambiguous. The aryl hydrocarbon receptor (AHR) is a ligand-activated transcription factor that activates detoxifying pathways with numerous exogenous ligands, including tobacco smoke. Whereas transient AHR activation is adaptive, chronic activation can be toxic. On this basis, we tested the hypothesis that chronic smoke-induced AHR activation causes adverse muscle impact. MethodsWe used clinical patient muscle samples, and in vitro (C2C12 myotubes) and in vivo models (mouse), to perform gene expression, mitochondrial function, muscle and neuromuscular junction morphology, and genetic manipulations (adeno-associated virus-mediated gene transfer). Results16 weeks tobacco smoke exposure in mice caused: muscle atrophy, neuromuscular junction degeneration, and reduced oxidative capacity. Similarly, smoke exposure reprogrammed the muscle transcriptome, with down-regulation of mitochondrial and neuromuscular junction genes. In mouse and human patient specimens, smoke exposure increased muscle AHR signaling. Mechanistically, experiments in cultured myotubes demonstrated that smoke condensate activated the AHR, caused mitochondrial impairments, and induced an AHR-dependent myotube atrophy. Finally, to isolate the role of AHR activity, expression of a constitutively active AHR mutant without smoke exposure caused atrophy and mitochondrial impairments in cultured myotubes, and muscle atrophy and neuromuscular junction degeneration in mice. ConclusionsThese results establish that chronic AHR activity, as occurs in smokers, phenocopies the atrophy, mitochondrial impairment and neuromuscular junction degeneration caused by chronic tobacco smoke exposure.

physiology↗

Mitochondrial PE potentiates respiratory enzymes to amplify skeletal muscle aerobic capacity

Exercise capacity is a strong predictor of all-cause mortality. Skeletal muscle mitochondrial respiratory capacity, its biggest contributor, adapts robustly to changes in energy demands induced by contractile activity. While transcriptional regulation of mitochondrial enzymes has been extensively studied, there is limited information on how mitochondrial membrane lipids are regulated. Herein, we show that exercise training or muscle disuse alters mitochondrial membrane phospholipids including phosphatidylethanolamine (PE). Addition of PE promoted, whereas removal of PE diminished, mitochondrial respiratory capacity. Surprisingly, skeletal muscle-specific inhibition of mitochondrial-autonomous synthesis of PE caused a respiratory failure due to metabolic insults in the diaphragm muscle. While mitochondrial PE deficiency coincided with increased oxidative stress, neutralization of the latter did not rescue lethality. These findings highlight the previously underappreciated role of mitochondrial membrane phospholipids in dynamically controlling skeletal muscle energetics and function.

physiology↗