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Investigating the roles of epicardial fat and long-chain acylcarnitines in cardio-metabolic disease
Doctoral Thesis   Open access

Investigating the roles of epicardial fat and long-chain acylcarnitines in cardio-metabolic disease

Hamish Michael Aitken-Buck and Hamish Michael Aitken-Buck
Doctor of Philosophy - PhD, University of Otago
University of Otago
2021
Handle:
https://hdl.handle.net/10523/12531

Abstract

New Zealand Epicardial adipose tissue Obesity Long-chain acylcarnitines Calcium Ryanodine receptor Cardiovascular disease
Heart fat, termed epicardial adipose tissue (EAT), expands in cardio-metabolic disease; however, whether hypertrophy of the comprising adipocytes underlies this expansion is unknown. Part one of my thesis aimed to examine the relationship between EAT adipocyte size, macroscopic EAT thickness, and obesity level. I also investigated the role of EAT adipocytokine release in cardiovascular pathogenesis by determining the effect of the EAT-derived factor, resistin, on human myocardium function. EAT adipocytes were measured in histological sections of EAT procured from post-mortem case (N=43) and surgery patient (N=49) cohorts. In each cohort, EAT adipocyte size did not correlate with the obesity measure, body mass index (BMI) (post-mortem cohort: r=0.1, P=0.4; surgery cohort: r=0.1, P=0.5), despite finding a positive correlation for paired subcutaneous adipocytes (r=0.6, P<0.0001). Furthermore, in the surgery cohort, adipocyte size did not correlate with EAT thickness (r=-0.1, P=0.6). Exploratory analysis of adipocyte size frequency distributions indicated that EAT from obese cases contains a greater proportion of ‘smaller’ adipocytes. Enzyme-linked immunosorbent assay revealed that human EAT (N=36) releases resistin. When applied to human atrial trabeculae (N=10), exogenous resistin (7, 12, 20 ng/mL) did not change the propensity for spontaneous muscle contractions. Resistin did, however, dose-dependently increase trabeculae contractility (maximal 2.9-fold increase, P<0.0001), while also reducing post-pause contraction potentiation (maximal 2-fold decrease, P=0.002). These data suggest that expansion of EAT in obesity might be associated with hyperplastic, and not hypertrophic, remodelling of EAT adipocytes. Additionally, the findings suggest that resistin released from EAT exerts a direct inotropic, but not an arrhythmogenic, effect on human myocardium. Circulating levels of the metabolites, long-chain acylcarnitines (LCACs), are associated with CVD risk. Part two of my thesis sought to determine if LCACs also directly alter cellular Ca2+ handling and human myocardial function. Human atrial trabeculae were stimulated at 60 contractions per minute and treated with LCAC species 18:1 (1-25 µM, n=8 per concentration). LCAC 18:1 dose-dependently increased contractility (maximal 1.5-fold increase, P<0.01) and increased arrhythmic contraction propensity (maximal 50% increase, P<0.05). To investigate LCAC effects on Ca2+ handling, human embryonic kidney cells with inducible ryanodine receptor (RyR2) expression were loaded with the cytosolic Ca2+ indicator, fluo-4-AM, or the intra-endoplasmic reticulum Ca2+ indicator, D1ER. All LCAC 18:1 concentrations tested (0.1-25 µM) promoted spontaneous Ca2+ release events by reducing the threshold for RyR2-mediated Ca2+ release (89% of control, P<0.0001). In addition to promoting spontaneous Ca2+ release, higher LCAC 18:1 concentrations also markedly increased the rates of Ca2+ and Zn2+ influx (maximal 3- to 7-fold increases, P<0.0001) from the extracellular environment. Treatment with a different LCAC, LCAC 16:0, induced analogous effects on Ca2+ release, Ca2+ influx, and Zn2+ influx, but to a lesser extent than that induced by LCAC 18:1, suggesting that fatty acyl chain and likely membrane disruption underlies the effects of LCACs. Circulating LCACs directly alter human myocardium function. In vitro, this is linked to LCAC-induced membrane perturbation that promotes Ca2+ influx and enhances spontaneous RyR2 Ca2+ release. This suggests that high LCACs levels might contribute to cardiovascular pathogenesis in addition to offering diagnostic utility.
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