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An Evaluation of the Impacts of Aging on Skeletal Muscle

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An Evaluation of the Impacts of Aging on Skeletal Muscle AN EVALUATION OF THE IMPACTS OF AGING ON SKELETAL MUSCLE PERFORMANCE IN SEVERAL MAMMALIAN DIVERS A Dissertation by ALLYSON GAYLE HINDLE Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY December 2007 Major Subject: Wildlife and Fisheries Sciences AN EVALUATION OF THE IMPACTS OF AGING ON SKELETAL MUSCLE PERFORMANCE IN SEVERAL MAMMALIAN DIVERS A Dissertation by ALLYSON GAYLE HINDLE Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Approved by: Co-Chairs of Committee, M. Horning R.W. Davis Committee Members, W.H. Neill D.S. MacKenzie J.M. Lawler Head of Department, T.E. Lacher December 2007 Major Subject: Wildlife and Fisheries Sciences iii ABSTRACT An Evaluation of the Impacts of Aging on Skeletal Muscle Performance in Several Mammalian Divers. (December 2007) Allyson Gayle Hindle, B.S., University of Manitoba; M.S. University of Manitoba Co-Chairs of Advisory Committee: Dr. M. Horning Dr. R. Davis Based on the ‘free radical theory of aging,’ I hypothesized that hypoxia caused by the mammalian dive response induces free radical production which could modulate or accelerate cellular aging. On the other hand, to prevent free radical “stress” (pro- /antioxidant imbalance), divers could display elevated protective mechanisms. Additionally, the unusual connection between diving physiology and foraging ecology implies that aging physiology is significant to our understanding of ecology for divers. This study examines three aspects of aging in representative diving mammals. First, gracilis muscle morphology was analyzed for old/young shrews (water shrew, Sorex palustris (diver); short-tailed shrew, Blarina brevicauda (non-diver)). Extracellular space was elevated in old animals (10% diver, ~70% non-diver; P=0.021), which corresponded to a larger extracellular collagen component of old muscle (~60%; P=0.008). Muscle was dominated by Type I collagen, and the ratio of collagen Type I: III more than doubled with age (P=0.001). Second, oxidative stress markers, protective antioxidant enzymes and apoptosis were examined in muscle of the two shrew species. The activities of antioxidant iv enzymes catalase and glutathione peroxidase were statistically identical at each age in both species. The Cu,Zn superoxide dismutase isoform was, however, elevated in older animals (115% diver, 83% non-diver, P=0.054). Only one indicator of oxidative stress (lipid peroxidation) increased with age (P=0.009), whereas the other markers declined (4-hydroxynonenal content, P=0.008, dihydroethidium oxidation, P=0.025). Apoptosis occurred in <1% of myocytes, and did not change with age. On balance, diving water shrews did not have adaptations to combat oxidative stress, yet they do not display excessive oxidative tissue damage. Apoptosis was similar between species. The third study component was the development of a predictive simulation model for the energetics of old/young foraging Weddell seals, Leptonychotes weddellii. With advancing age, the model predicts declining net energy gain associated with a decrease in muscle contractile efficiency. The effects of age are exacerbated when good prey patches are scarce. In such cases, declines in old seal energy gain caused by increased buoyancy and decreased aerobic dive limit become apparent. The model also addresses the idea that behavioral plasticity may allow older animals to compensate for age-related performance constraints. v NOMENCLATURE 4-HNE 4-hydroxynonenal Adive Respiratory costs of diving ADL Aerobic dive limit Afecal (Af) fecal production cost; energy not assimilated Amyocyte Average myocyte cross-sectional area Arespiratory (Ar) total respiratory cost Asurface Respiratory costs at the surface Atotal Total area of section Aurinary (Au) cost of urinary production; energy not assimilated Awaste (Aw) total cost of waste production BMR Basal metabolic rate BSA Bovine serum albumin cADL Calculated aerobic dive limit CAT Catalase CS Citrate synthase DD Dive duration DHE Dihydroethidium D:S Dive: surface duration ratio ECM Extracellular matrix ECS Extracellular space EDL Extensor digitorum longus vi Eexpended Simulated daily energy expenditure Egained Simulated daily energy intake FOX Ferrous oxide xylenol orange assay GPx Glutathione peroxidase GSH Reduced glutathione HIF Heat increment of feeding IGF-1 Insulin-like growth factor 1 Km Substrate concentration at ½ Vmax LDH Lactate dehydrogenase MHC Myosin heavy chain MMP Matrix metalloprotease MR Metabolic rate · NO Nitric oxide ·- O2 Superoxide radical ONOO- Peroxynitrite P Environmental prey density PBS Phosphate buffered saline PDST Post-dive surface time r myocyte Myocyte density in area Pthreshold Prey threshold for bout diving ROS Reactive oxygen species RNS Reactive nitrogen species vii SOD Superoxide dismutase STS Short-tailed shrew TBS Tris buffered saline TUNEL Terminal transferase dUTP nick-end labeling Vmax Maximum velocity of an enzyme-catalyzed reaction VO2 Volume of oxygen consumed VO2max Maximum volume of oxygen which can be consumed WS Water shrew viii TABLE OF CONTENTS Page ABSTRACT ..................................................................................................................... iii NOMENCLATURE ...........................................................................................................v TABLE OF CONTENTS ............................................................................................... viii LIST OF TABLES ............................................................................................................xi LIST OF FIGURES..........................................................................................................xii 1. INTRODUCTION........................................................................................................1 Literature Review......................................................................................................1 Skeletal Muscle Aging ...........................................................................................1 Reactive Oxygen Species in Mammalian Skeletal Muscle....................................3 Aging in Wild Populations .....................................................................................6 Reactive Oxygen Species and Senescence in Diving Mammals............................9 Study Objectives...................................................................................................12 2. AGE EFFECTS ON DIVE BEHAVIOR AND THE ENERGY BUDGET OF A SIMULATED WEDDELL SEAL..............................................................................14 Introduction.............................................................................................................14 Aging in Marine Mammals ..................................................................................14 Model Background ...............................................................................................16 Exercise Physiology and Aging ...........................................................................17 Materials and Methods ............................................................................................20 Conceptual Model Overview and Assumptions ...................................................20 Mechanistic Overview..........................................................................................21 Daily Energy Budget............................................................................................23 Dive Predictions and Prey Encounter...................................................................26 Age-Related Changes ...........................................................................................29 Available Model Outputs .....................................................................................31 Objectives.............................................................................................................31 Results .....................................................................................................................33 Evaluation of Simulation System Dynamics with Respect to Natural System....33 Sensitivity Analysis..............................................................................................38 Effect of Simulated Aging on Diving and the Energy Budget.............................41 Discussion ...............................................................................................................47 Applicability of the Model ...................................................................................47 ix Page Functionality of the Model ...................................................................................48 Effect of Prey Condition and Simulated Aging on Diving and the Energy Budget ..................................................................................................................50 Model Predictions and Conclusions .....................................................................54 3. HISTOLOGICAL CHANGES IN AGING MUSCLE IN TWO SPECIES OF SHREW......................................................................................................................56 Introduction.............................................................................................................56 Materials and Methods ............................................................................................59
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