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ABSTRACT: Transmembrane lactate movements are mediated by monocarboxylate transporters (MCTs), but these proteins have never been characterized in rainbow trout. Our goals were to clone potential trout MCTs, determine tissue distribution, and quantify the effects of exhausting exercise on MCT expression. Such information could prove important to understand the mechanisms underlying the classic "lactate retention" seen in trout white muscle after intense exercise. Four isoforms were identified and partially characterized in rainbow trout: MCT1a, MCT1b, MCT2, and MCT4. MCT1b was the most abundant in heart, and red muscle, but poorly expressed in gill and brain where MCT1a and MCT2 were prevalent. MCT expression was strongly stimulated by exhausting exercise in brain (MCT2: +260%) and heart (MCT1a: +90% and MCT1b: +50%), possibly to increase capacity for lactate uptake in these highly oxidative tissues. By contrast, the MCTs of gill, liver and muscle remained unaffected by exercise. This study provides a possible functional explanation for post-exercise "lactate retention" in trout white muscle. Rainbow trout may be unable to release large lactate loads rapidly during recovery because: (i) they only poorly express MCT4, the main lactate exporter found in mammalian glycolytic muscles, (ii) the combined expression of all trout MCTs is much lower in white muscle than in any other tissue, and (iii) exhausting exercise fails to upregulate white muscle MCT expression. In this tissue, carbohydrates act as an "energy spring" that alternates between explosive power release during intense swimming (glycogen to lactate) and recoil during protracted recovery (slow glycogen resynthesis from local lactate).
AJP Regulatory Integrative and Comparative Physiology 03/2013; · 3.34 Impact Factor
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ABSTRACT: The effects of short-term food deprivation on lipid metabolism are well documented, but little is known about prolonged fasting. This study monitored the kinetics of glycerol (rate of appearance, R(a) glycerol) and non-esterified fatty acids (R(a) NEFA) in fasting rabbits. Our goals were to determine whether lipolysis is stimulated beyond values seen for short-term fasting, and to characterize the roles of primary (intracellular) and secondary (with transit through the circulation) triacylglycerol/fatty acid cycling (TAG/FA cycling) in regulating fatty acid allocation to oxidation or re-esterification. R(a) glycerol (9.62±0.72 to 15.29±0.96 μmol kg(-1) min(-1)) and R(a) NEFA (18.05±2.55 to 31.25±1.93 μmol kg(-1) min(-1)) were stimulated during the first 2 days of fasting, but returned to baseline after 4 days. An initial increase in TAG/FA cycling was followed by a reduction below baseline after 6 days without food, with primary and secondary cycling contributing to these responses. We conclude that the classic activation of lipolysis caused by short-term fasting is abolished when food deprivation is prolonged. High rates of re-esterification may become impossible to sustain, and TAG/FA cycling could decrease to reduce its cost to 3% of total energy expenditure. Throughout prolonged fasting, fatty acid metabolism gradually shifts towards increased oxidation and reduced re-esterification. Survival is achieved by pressing fuel selection towards the fatty acid dominance of energy metabolism and by slowing substrate cycles to assist metabolic suppression. However, TAG/FA cycling remains active even after prolonged fasting, suggesting that re-esterification is a crucial mechanism that cannot be stopped without harmful consequences.
Journal of Experimental Biology 05/2012; 215(Pt 9):1484-90. · 3.00 Impact Factor
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Jean-Michel Weber
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ABSTRACT: Animals must regulate the fluxes of multiple fuels to support changing metabolic rates that result from variation in physiological circumstances. The aim of fuel selection strategies is to exploit the advantages of individual substrates while minimizing the impact of disadvantages. All exercising mammals share a general pattern of fuel selection: at the same %V(O(2,max)) they oxidize the same ratio of lipids to carbohydrates. However, highly aerobic species rely more on intramuscular fuels because energy supply from the circulation is constrained by trans-sarcolemmal transfer. Fuel selection is performed by recruiting different muscles, different fibers within the same muscles or different pathways within the same fibers. Electromyographic analyses show that shivering humans can modulate carbohydrate oxidation either through the selective recruitment of type II fibers within the same muscles or by regulating pathway recruitment within type I fibers. The selection patterns of shivering and exercise are different: at the same %V(O(2,max)), a muscle producing only heat (shivering) or significant movement (exercise) strikes a different balance between lipid and carbohydrate oxidation. Long-distance migrants provide an excellent model to characterize how to increase maximal substrate fluxes. High lipid fluxes are achieved through the coordinated upregulation of mobilization, transport and oxidation by activating enzymes, lipid-solubilizing proteins and membrane transporters. These endurance athletes support record lipolytic rates in adipocytes, use lipoprotein shuttles to accelerate transport and show increased capacity for lipid oxidation in muscle mitochondria. Some migrant birds use dietary omega-3 fatty acids as performance-enhancing agents to boost their ability to process lipids. These dietary fatty acids become incorporated in membrane phospholipids and bind to peroxisome proliferator-activated receptors to activate membrane proteins and modify gene expression.
Journal of Experimental Biology 01/2011; 214(Pt 2):286-94. · 3.00 Impact Factor
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ABSTRACT: Current understanding of lactate metabolism in fish is based almost entirely on the interpretation of concentration measurements that cannot be used to infer changes in flux. The goals of this investigation were: (1) to quantify baseline lactate fluxes in rainbow trout (Oncorhynchus mykiss) under normoxic conditions; (2) to establish how changes in rates of lactate appearance (R(a)) and disposal (R(d)) account for the increase in blood lactate elicited by hypoxia; and (3) to identify the tissues responsible for lactate production. R(a) and R(d) lactate of rainbow trout were measured in vivo by continuous infusion of [U-(14)C]lactate in trout exposed to 25% O(2) saturation or maintained in normoxia for 90 min. In normoxic fish, R(a) lactate decreased from 18.2 to 13.1 μmol kg(-1) min(-1) and R(d) lactate from 19.0 to 12.8. R(a) and R(d) were always matched, thereby maintaining a steady baseline blood lactate concentration of ∼0.8 mmol l(-1). By contrast, the hypoxic fish increased blood lactate to 8.9 mmol l(-1) and R(a) lactate from 18.4 to 36.5 μmol kg(-1) min(-1). This stimulation of anaerobic glycolysis was unexpectedly accompanied by a 52% increase in R(d) lactate from 19.9 to 30.3 μmol kg(-1) min(-1). White muscle was the main producer of lactate, which accumulated to 19.2 μmol g(-1) in this tissue. This first study of non-steady-state lactate kinetics in fish shows that the increase in lactate disposal elicited by hypoxia plays a strategic role in reducing the lactate load on the circulation. Without this crucial response, blood lactate accumulation would double.
Journal of Experimental Biology 11/2010; 213(Pt 22):3802-9. · 3.00 Impact Factor
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ABSTRACT: Seabirds differ dramatically in life history traits and breeding strategies. For example, gulls have short incubation shifts (several hours) and high metabolic rates, auks have medium-length incubation shifts (12-24h) and high metabolic rates, and petrels have long incubation shifts (days) and low metabolic rates. How these different strategies affect the dynamics of body components is poorly known. We compared body, organ and lipid mass changes among three different seabirds (gull: black-legged kittiwake Rissa tridactyla; auk: thick-billed murre Uria lomvia; petrel: northern fulmar Fulmarus glacialis) at Prince Leopold Island, Nunavut, Canada during 2002 (a year with low reproductive success and poor chick growth across all three species). This study is among the first to compare mass and lipid dynamics among different species foraging in the same food web and at similar trophic levels during the same breeding season (same environmental conditions). In fulmars and murres, most of decreases in body mass reflected decreases in lipid mass while in kittiwakes the increase in body mass reflected an increase in lean mass, especially the muscle. The species with the longest fasting endurance (incubation shift length) had the highest percent body lipids during incubation (fulmars: 13.3%, murres: 7.3%, kittiwakes: 6.9%), the highest variability in body lipids, tended to regulate body mass primarily through lipid stores and tended to regulate exercise and digestive organs separately. In contrast, in the species with the highest metabolic rate, all organ systems were adjusted similarly and in relation to body mass, and in a similar manner between incubation (stress due to heavy ice conditions) and chick-rearing (lower stress due to ice-free conditions). In high metabolic rate species, we suggest that organ size varies in response to environmental stress. We conclude that the organ dynamics of seabirds are set by a combination of key life history traits (like incubation shift and metabolic rate) and environmental conditions.
Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology 09/2010; 158(1):77-82. · 1.61 Impact Factor
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ABSTRACT: This study characterizes the effects of shivering thermogenesis on metabolic fuel selection in Wistar rats. Because lipids account for most of the heat produced, we have investigated: (1) whether the rate of appearance of non-esterified fatty acids (R(a) NEFAs) is stimulated by shivering, (2) whether mono-unsaturated (oleate) and saturated fatty acids (palmitate) are affected similarly, and (3) whether the partitioning between fatty acid oxidation and re-esterification is altered by cold exposure. Fuel oxidation was measured by indirect calorimetry and fatty acid mobilization by continuous infusion of 9,10-[(3)H]oleate and 1-[(14)C]palmitate. During steady-state cold exposure, results show that total heat production is unequally shared by the oxidation of lipids (52% of metabolic rate), carbohydrates (35%) and proteins (13%), and that the same fuel selection pattern is observed at all shivering intensities. All previous research shows that mammals stimulate R(a) NEFA to support exercise or shivering. In contrast, results reveal that the R(a) NEFA of the rat remains constant during cold exposure (55 micromol kg(1) min(1)). No preferential use of mono-unsaturated over saturated fatty acids could be demonstrated. The rat decreases its rate of fatty acid re-esterification from 48.4 +/- 6.4 to 19.6 +/- 6.3 micromol kg(1) min(1) to provide energy to shivering muscles. This study is the first to show that mammals do not only increase fatty acid availability for oxidation by stimulating R(a) NEFA. Reallocation of fatty acids from re-esterification to oxidation is a novel, alternative strategy used by the rat to support shivering.
The Journal of Physiology 08/2009; 587(Pt 17):4349-59. · 4.72 Impact Factor
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ABSTRACT: The laying of smaller replacement eggs has been described as a time-saving adaptation because chicks generally grow faster once hatched than inside the egg. However, chicks hatched from smaller eggs have, potentially, lower survival. Consequently, the smaller replacement egg represents a benefit to the female in terms of preserving its own condition at a cost to their offspring. We test these ideas by measuring adult mass changes and plasma lipid concentration changes in male and female Brünnich's guillemots Uria lomvia breeding on Coats Island, Nunavut. Though males lost more mass than females, these differences were not significant. Between laying the first and replacement egg, plasma fatty acid concentrations declined in females and increased in males, suggesting that females mobilise less lipid to preserve their condition after laying the replacement egg. In females, plasma lipid concentrations of the dominant fatty acids found in the eggs (16:0 and 18:1) declined between the laying of first and replacement eggs while plasma concentrations of 20:1 increased in both males and females. We compared the fatty acid signatures of first and replacement egg to look for evidence of differences between the lipid sources for their production. Principal component and discriminant function analyses showed that the fatty acid signatures of replacement eggs were closer to the signatures of the local prey than those of first eggs. We suggest that females rely on local sources of energy to a greater degree for the production of the replacement egg than the first egg, but that endogenous reserves of certain nutrients are important for the production of both eggs.
Journal of Avian Biology 05/2009; 40(3):327 - 336. · 2.28 Impact Factor
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ABSTRACT: Wild semipalmated sandpipers (Calidris pusilla) eat n-3 fatty acids to prime their muscles for long migrations. Sedentary bobwhite quails (Colinus virginianus) were used as a model to investigate the mechanisms for this natural doping. Our goal was to characterize the stimulating effects of n-3 eicosapentaenoic acid (EPA) and n-3 docosahexaenoic acid (DHA) on oxidative capacity. Mechanisms linked to changes in membrane composition and in gene expression for peroxisome proliferator-activated receptors (PPAR) were investigated. Dietary n-3 fatty acids stimulated the activities of oxidative enzymes by 58-90% (citrate synthase, cytochrome oxidase, carnitine palmitoyl transferase and hydroxyacyl dehydrogenase), and sedentary quails showed the same changes in membrane composition as sandpipers preparing for migration. EPA and DHA have the same doping effect. The substitution of n-6 arachidonic acid by n-3 EPA in membrane phospholipids plays an important role in mediating the metabolic effects of the diet, but results provide no significant support for the involvement of PPARs (as determined by changes in gene expression). The fatty acid composition of mitochondrial membranes and sarcoplasmic reticulum can be monitored by measuring total muscle phospholipids because all phospholipids are equally affected by diet. Only extreme regimes of endurance training can lead to increments in oxidative capacity matching those induced here by diet. As they prepare for long migrations, semipalmated sandpipers improve their physical fitness by eating! Choosing n-3 fatty acid doping over endurance training strikes us as a better strategy to boost aerobic capacity when rapid storage of energy is critical.
Journal of Experimental Biology 05/2009; 212(Pt 8):1106-14. · 3.00 Impact Factor
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Jean-Michel Weber
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ABSTRACT: Long-distance migrants have evolved specific adaptations that make their athletic records possible. Unique mechanisms explaining their amazing capacity for endurance exercise have now been uncovered, particularly with respect to energy storage, mobilization, transport and utilization. Birds are champions of migration because flying offers a key compromise: it allows more rapid movement than swimming, but has a lower cost of transport than running. High efficiency for muscle contraction, pointed wings, low wingloading, travelling in V-formations, storing fuel as energy-dense lipids and atrophy of non-essential organs are some of their strategies to decrease the cost of transport. The ability to process lipids rapidly also emerges as a crucial component of the migrant phenotype. High lipid fluxes are made possible by lipoprotein shuttles and fatty acid binding proteins (FABPs) that accelerate lipid transport and by upgrading the metabolic machinery for lipolysis and lipid oxidation. Preparation for long flights can include natural doping on n-3 polyunsaturated fatty acids (n-3 PUFAs) from unique invertebrate diets. Muscle performance is improved by restructuring membrane phospholipids and by activating key genes of lipid metabolism through peroxisome proliferator-activated receptors (PPARs). The physiological secret to long migrations does not depend on a single ;magic' adaptation but on the integration of multiple adjustments in morphology, biomechanics, behavior, nutrition and metabolism. Research on the physiology of migrants improves the fundamental knowledge of exercise biology, but it also has important implications for wildlife conservation, treating obesity and improving the performance of human athletes.
Journal of Experimental Biology 04/2009; 212(Pt 5):593-7. · 3.00 Impact Factor
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ABSTRACT: Lipolysis provides fatty acids that support key life processes by functioning as membrane components, oxidative fuels and metabolic signals. It is commonly measured as the rate of appearance of glycerol (Ra glycerol). Its in vivo regulation by catecholamines has been thoroughly investigated in mammals, but little information is available for ectotherms. Therefore, the goals of this study were, first, to characterize the effects of the catecholamines norepinephrine (NE) and epinephrine (Epi) on the lipolytic rate of intact rainbow trout (Oncorhynchus mykiss) and, second, to determine whether the plasma glycerol concentration is a reliable index of Ra glycerol. Our results show that baseline Ra glycerol (4.6+/-0.4 micromol kg(-1) min(-1)) is inhibited by NE (-56%), instead of being stimulated, as in mammals, whereas Epi has the same activating effect in both groups of vertebrates (+167%). NE-induced inhibition of fish lipolysis might play a particularly important role during aquatic hypoxia, when survival often depends on regulated metabolic depression. The plasma glycerol concentration is a poor predictor of Ra glycerol, and it should not be used as an index of lipolysis. Trout maintain a particularly high baseline lipolytic rate because only 13% of the fatty acids provided are sufficient to support total energy expenditure, whereas the remaining fatty acids must undergo reesterification (87%).
Journal of Experimental Biology 09/2008; 211(Pt 15):2460-6. · 3.00 Impact Factor
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ABSTRACT: Fish may use lipoproteins instead of albumin-bound fatty acids to fuel endurance exercise, but lipoprotein kinetics have never been measured in ectotherms. In vivo bolus injections of labeled very-low-density lipoproteins ((3)H-VLDL labeled in vivo from donor fish) and continuous infusions of Intralipid (3H-labeled artificial emulsion) were used to investigate the effects of prolonged exercise (6 h at 1.5 body length/s) and heparin (600 U/kg) on the turnover rate of circulating triacylglycerol (TAG) in rainbow trout. We hypothesized that swimming would stimulate TAG turnover rate to fuel working muscles and that heparin would reduce flux by releasing lipoprotein lipase (LPL) from endothelial cells. Results from both tracer methods show that the baseline TAG turnover rate of trout ranges from 24 to 49 mumol TAG.kg(-1) x min(-1) and exceeds all values measured to date in endotherms. More important, this high resting turnover rate is not stimulated during swimming, because it can already cover several times the energy requirements of locomotion. The fact that heparin causes a 50% decrease in baseline TAG turnover rate suggests that fish LPL must be bound to the endothelium for normal tissue uptake of fatty acids supplied by lipoproteins, as in mammals. We propose that the high resting TAG turnover rate of rainbow trout could be needed by ectotherms for rapid restructuring of membrane phospholipids. The continuous tracer infusion method implemented here could be a versatile tool to investigate the potential role of lipoproteins in providing fatty acids for rapid homeoviscous adaptation.
AJP Regulatory Integrative and Comparative Physiology 08/2008; 295(1):R309-15. · 3.34 Impact Factor
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ABSTRACT: Fish endurance swimming is primarily powered by lipids supplied to red muscle by the circulation, but the mechanism of delivery remains unknown. By analogy to mammals, previous studies have focused on non-esterified fatty acids (NEFA bound to albumin), but lipoproteins have not been considered as an energy shuttle to working muscles. The effects of exercise on fish lipoprotein lipase (LPL) have never been investigated. We hypothesized that LPL and circulating lipoproteins would be modified by prolonged swimming. Because LPL is naturally bound to the endothelium, we have used heparin to release the enzyme in the circulation and to characterize reserve capacity for lipoprotein catabolism. The effects of exercise (4 days at 1.5 body lengths s(-1) in a swim tunnel) were measured for red muscle LPL, post-heparin plasma LPL, and lipoprotein concentration/composition. Red muscle LPL activity increased from 18+/-5 (rest) to 49+/- 9 nmol fatty acids min(-1) g(-1) (swimming). In resting fish, heparin administration caused a 27-fold increase in plasma LPL activity that reached a maximum of 1.32+/- 0.67 micromol fatty acids min(-1) ml(-1) plasma. This heparin-induced response of plasma LPL was not different between resting controls and exercised fish. Heparin or prolonged swimming had no effect on the concentration/composition of lipoproteins that contain 92% of the energy in total plasma lipids. We conclude that (1) red muscle LPL is strongly activated by endurance swimming, (2) rainbow trout have a high reserve capacity for hydrolyzing lipoproteins, and (3) future studies should aim to measure lipoprotein flux because their concentration does not reflect changes in flux. These novel characteristics of fish LPL imply that lipoproteins are used as a metabolic shuttle between fat reserves and working muscles, a strategy exploiting an abundant source of energy in rainbow trout.
Journal of Experimental Biology 12/2007; 210(Pt 22):4016-23. · 3.00 Impact Factor
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ABSTRACT: For long migrations, birds must rely on high flux capacities at all steps of lipid metabolism, from the mobilization of adipose reserves to fatty acid oxidation in flight muscle mitochondria. Substrate kinetics and indirect calorimetry were used to investigate key parameters of lipid metabolism in a highly aerobic shorebird: the ruff sandpiper Philomachus pugnax. In this study, we have quantified the effects of cold exposure because such measurements are presently impossible during flight. Lipolytic rate was monitored by continuous infusion of 2-[(3)H]-glycerol and lipid oxidation by respirometry. Plasma lipid concentrations (non-esterified fatty acids, neutral lipids and phospholipids) and their fatty acid composition were also measured to assess whether cold exposure causes selective metabolism of specific lipids. Results show that shivering leads to a 47% increase in metabolic rate (44.4+/-3.8 ml O(2)kg(-1) min(-1) to 65.2+/-8.1 ml O(2) kg(-1) min(-1)), almost solely by stimulating lipid oxidation (33.3+/- 3.3 ml O(2) kg(-1) min(-1) to 48.2+/-6.8 ml O(2) kg(-1) min(-1)) because carbohydrate oxidation remains close to 11.5+/- 0.5 ml O(2) kg(-1) min(-1). Sandpipers support an unusually high lipolytic rate of 55-60 micromol glycerol kg(-1) min(-1). Its stimulation above thermoneutral rates is unnecessary during shivering when the birds are still able to re-esterify 50% of released fatty acids. No changes in plasma lipid composition were observed, suggesting that cold exposure does not lead to selective metabolism of particular fatty acids. This study provides the first measurements of lipolytic rate in migrant birds and shows that their capacity for lipid mobilization reaches the highest values measured to date in vertebrates. Extending the limits of conventional lipid metabolism has clearly been necessary to achieve long-distance migrations.
Journal of Experimental Biology 05/2007; 210(Pt 7):1161-9. · 3.00 Impact Factor
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ABSTRACT: During their fall migration from the Arctic to South America, semipalmated sandpipers Calidris pusilla stop in the Bay of Fundy (east coast of Canada) before flying non-stop for approximately 4500 km across the ocean. Refueling birds double their body mass by feeding on Corophium volutator, an amphipod containing high amounts of n-3 polyunsaturated fatty acids (n-3 PUFA), particularly eicosapentaenoic (20:5) and docosahexaenoic acid (22:6). In mammals, high dietary intake of n-3 PUFA is known to increase capacity for oxidative metabolism. Therefore, we hypothesized that tissue incorporation of n-3 PUFA would be associated with increases in the activity of key muscle enzymes to upregulate energy metabolism for prolonged exercise. Birds were collected at various stages of fat loading to monitor changes in lipid composition and flight muscle enzymes simultaneously. Enzymes were measured to assess oxidative capacity [citrate synthase (CS)], beta-oxidation [carnitine palmitoyl transferase (CPT) and 3-hydroxyacyl dehydrogenase (HOAD)] and glycolytic capacity [lactate dehydrogenase (LDH)]. Changes in the fatty acid composition of muscle membranes (phospholipids) and fuel reserves (neutral lipids) were measured separately to distinguish between membrane-related and systemic effects of n-3 PUFA. Results show that muscle CS and HOAD are stimulated during refueling and that their activities are correlated with n-3 PUFA content in phospholipids (22:6 for CS, 20:5 for HOAD) and in neutral lipids (20:5 for CS). This suggests that 20:5 and 22:6 have different effects on energy metabolism and that they act via changes in membrane structure and systemic mechanisms. CPT and LDH did not change during refueling, but LDH activity was significantly related to the n-3 PUFA content of fuel reserves. This study shows that oxidative capacity increases rapidly during refueling and supports the idea that dietary n-3 PUFA are used as molecular signals to prime flight muscles of some long-distance migrants for extreme exercise.
Journal of Experimental Biology 03/2007; 210(Pt 3):413-20. · 3.00 Impact Factor
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ABSTRACT: Chronic omega-3 or omega-6 polyunsaturated fatty acid (n-3; n-6 respectively) treatment attenuated human interleukin-1beta (hIL-1beta; 5.0 microg/kg)-elicited rise of circulating ACTH levels and attenuated the sickness behavior and locomotor suppression elicited by the cytokine. Furthermore, hIL-1beta markedly elevated circulating levels of plasma IL-6, an effect attenuated by n-3, but not n-6 treatment. Such protective effects were not evident upon short-term (3 day) n-3 exposure. These results demonstrate that long-term administration of either n-3 or n-6 confers protection against several neuroendocrinological, immunological and behavioral actions of hIL-1beta challenge, although in general the effects of n-3 were more pronounced.
Journal of Neuroimmunology 01/2007; 181(1-2):19-28. · 2.96 Impact Factor
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ABSTRACT: At the end of summer, semipalmated sandpipers (Calidris pusilla) traveling from the Arctic stop in the Bay of Fundy (east coast of Canada) to build large fat reserves before a non-stop flight to South America. During a 2-week stopover, the body mass of this small shorebird is doubled ( approximately 20 g to 40 g) by feeding on a burrowing amphipod, Corophium volutator, that contains unusually high levels of n-3 polyunsaturated fatty acids (PUFA). In mammals, high n-3 PUFA content of membrane phospholipids (PL) is linked to improved exercise performance due to increased membrane fluidity that accelerates transmembrane lipid transport. We hypothesized that dietary n-3 PUFA could be used as a natural ;performance-enhancing substance' by semipalmated sandpipers to prepare their flight muscles for migration. Also, PUFA stored as fuel in neutral lipids (NL) can be mobilized more quickly than saturated fatty acids, but they contain less energy per unit mass. It is therefore unclear whether dietary fatty acids are modified before storage. Birds were collected at various stages of fat loading to examine changes in the composition of tissue PL (membranes) and NL (fuel stores). Results show that dietary n-3 PUFA are incorporated in tissue lipids in less than 2 weeks. During the stopover, the double bond index of muscle PL increases by 25% and the fatty acid profiles of both muscle PL and adipose NL converge with that of the diet. However, >50% of dietary n-3 PUFA are converted to other fatty acids before storage, mainly to oleate (18:1), possibly because monounsaturates offer a compromise between high energy density and ease of mobilization. This study shows that long-distance migrant birds can (1) use natural diets rich in specific lipids to prime flight muscles for endurance exercise, and (2) modify dietary fatty acids before storing them as fuel.
Journal of Experimental Biology 07/2006; 209(Pt 14):2686-95. · 3.00 Impact Factor
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ABSTRACT: The effects of changes in shivering intensity on the relative contributions of plasma glucose, muscle glycogen, lipids and proteins to total heat production are unclear in humans. The goals of this study were: (1) to determine whether plasma glucose starts playing a more prominent role as shivering intensifies, (2) to quantify overall changes in fuel use in relation to the severity of cold exposure, and (3) to establish whether the fuel selection pattern of shivering is different from the classic fuel selection pattern of exercise. Using a combination of indirect calorimetry and stable isotope methodology, fuel metabolism was monitored in non-acclimatized adult men exposed for 90 mins to 10 degrees C (low-intensity shivering (L)) or 5 degrees C (moderate-intensity shivering (M)). Results show that plasma glucose oxidation is strongly stimulated by moderate shivering (+122% from L to M), but the relative contribution of this pathway to total heat generation always remains minor (< 15% of total heat production). Instead, muscle glycogen is responsible for most of the increase in heat production between L and M. By itself, the increase in CHO oxidation is responsible for the 100 W increase in metabolic rate observed between L and M, because rates of lipid and protein oxidation remain constant. This high reliance on CHO is not compatible with the well known fuel selection pattern of exercise, when considering the relatively low metabolic rates elicited by shivering (approximately 30% for M). We conclude that shivering and exercise of similar energy requirements appear to be supported by different fuel mixtures. Investigating the physiological mechanisms underlying why a muscle producing only heat (shivering), or significant movement (exercise), shows a different pattern of fuel selection at the same power output strikes us as a fascinating area for future research.
The Journal of Physiology 07/2005; 566(Pt 1):247-56. · 4.72 Impact Factor
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ABSTRACT: The metabolic consequences of cold exposure and exercise are not well characterized in birds. Ruff sandpipers Philomachus pugnax are migrant shorebirds traveling between Africa and Siberia for up to 30,000 km annually. Our goal was to quantify the fuel selection pattern of these remarkable athletes during shivering and terrestrial locomotion. We used indirect calorimetry and nitrogen excretion analysis to measure their rates of lipid, carbohydrate and protein oxidation at different temperatures (22, 15, 10 or 5 degrees C) and different treadmill speeds (15, 20, 25, 30, 35 or 40 m min(-1)). Results show that lipid oxidation supplies nearly all the energy necessary to support shivering and running, and that the pattern of oxidative fuel selection is independent of shivering or running intensity. During shivering, total ATP production is unequally shared between lipids (82%), carbohydrates (12%) and proteins (6%). During running, lipids remain the dominant substrate (66%), with carbohydrates (29%) and proteins (5%) playing more minor roles. The prevailing use of lipids during intense shivering and high-speed running is not consistent with the fuel selection pattern observed in exercising and cold-exposed mammals. The exact mechanisms allowing birds to use lipids at extremely high rates are still largely unexplored, and quantifying the relative importance of different fuels during long-distance flight remains a major challenge for future research.
Journal of Experimental Biology 02/2005; 208(Pt 2):317-25. · 3.00 Impact Factor
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ABSTRACT: The energy metabolism of hibernators has not been characterized for normothermic fasting, and our goal was to quantify oxidative fuel selection of non-hibernating woodchucks Marmota monax during prolonged food deprivation. Indirect calorimetry and nitrogen excretion measurements were used to assess changes in metabolic rate (VO2), fuel selection and composition of nitrogen wastes, as well as seasonal differences. For reference, matching experiments were also performed on rabbits. The results show that woodchucks have a higher metabolic rate in summer (271 micromol O2 kg(-1) min(-1)) than in spring (200 micromol O2 kg(-1) min(-1)) and that fasting-induced metabolic depression is only possible in summer (-25% in 14 days). The metabolic rate of rabbits is high at all times (383 micromol O2 kg(-1) min(-1)), but they show a more rapid depression in response to fasting (-32% in 7 days). Woodchucks have a naturally low reliance on proteins in the fed state (accounting for 8% VO2) in spring; 17% VO2 in summer; vs 28% VO2 in rabbits) and are able to decrease it even further during fasting (spring, 5% VO2); summer, 6% VO2; vs 20% VO2 in rabbits). This study shows that, apart from their notorious capacity for hibernation, woodchucks are particularly well adapted for normothermic fasting. Their ability to cope with prolonged food deprivation is based on a series of integrated responses eliciting deep metabolic depression and a rapid change in fuel selection to spare limited protein reserves. Information presently available on prolonged fasting suggests that such an ability for metabolic depression, possibly down to minimal levels still compatible with normothermic life, may be common among mammals. In contrast, the extreme protein sparing demonstrated in woodchucks is a unique metabolic feature of fasting champions.
Journal of Experimental Biology 01/2005; 207(Pt 26):4525-33. · 3.00 Impact Factor
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ABSTRACT: The thermogenic response of humans depends critically on the coordination of muscle fibre recruitment and oxidative fuel metabolism. The primary goal of this study was to determine whether the electromyographic (EMG) pattern of muscle recruitment could provide metabolic information on oxidative fuel selection during high-intensity shivering. EMG activity (of 8 large muscles) and fuel metabolism were monitored simultaneously in non-acclimatized adult men during high-intensity shivering. Even though acute cold exposure elicited similar changes in metabolic rate among subjects, lipid and carbohydrate use was very different. Depending on the subject, the cold-induced increase in carbohydrate (CHO) oxidation ranged between 2- and 8-fold, with CHO accounting for 33-78% of total heat production, and lipids for 14-60%. This high variability in fuel selection was primarily explained by differences in 'burst shivering' rate, indicating that the recruitment of type II fibres plays a key role in orchestrating fuel selection. This study is the first to show that the pattern of muscle recruitment can provide quantitative information on energy metabolism. Future work should focus on the study of shivering bursts that may provide essential clues on what limits human survival in the cold.
The Journal of Physiology 05/2004; 556(Pt 1):305-13. · 4.72 Impact Factor
