AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish,<i>Carassius auratus</i>

Jibb, Lindsay; Richards, Jeffrey G.

doi:10.1242/jeb.019117

Cited by 108 publications

(77 citation statements)

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“…and J.A.J., unpublished observations). Jibb and Richards (Jibb and Richards, 2008) show in their recent study that 0.5 h of hypoxia in goldfish leads to a 5.5-fold increase in AMPK activity in the liver. Consequently, we expect further studies to show that AMPK, as a central regulator of cellular energy metabolism, is involved in many kinds of stress response.…”

Section: Discussionmentioning

confidence: 97%

AMP-activated protein kinase (AMPK) in the rock crab,Cancer irroratus: an early indicator of temperature stress

Frederich

O'Rourke

Furey

et al. 2009

Journal of Experimental Biology

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SUMMARYExposure of marine invertebrates to high temperatures leads to a switch from aerobic to anaerobic metabolism, a drop in the cellular ATP concentration ([ATP]), and subsequent death. In mammals, AMP-activated protein kinase (AMPK) is a major regulator of cellular [ATP] and activates ATP-producing pathways, while inhibiting ATP-consuming pathways. We hypothesized that temperature stress in marine invertebrates activates AMPK to provide adequate concentrations of ATP at increased but sublethal temperatures and that AMPK consequently can serve as a stress indicator (similar to heat shock proteins, HSPs). We tested these hypotheses through two experiments with the rock crab, Cancer irroratus. First, crabs were exposed to a progressive temperature increase (6°C h -1 ) from 12 to 30°C. AMPK activity, total AMPK protein and HSP70 levels, reaction time, heart rate and lactate accumulation were measured in hearts at 2°C increments. AMPK activity remained constant between 12 and 18°C, but increased up to 9.1(±1.5)-fold between 18 and 30°C. The crabsʼ reaction time also decreased above 18°C. By contrast, HSP70 (total and inducible) and total AMPK protein expression levels did not vary significantly over this temperature range. Second, crabs were exposed for up to 6 h to the sublethal temperature of 26°C. This prolonged exposure led to a constant elevation of AMPK activity and levels of HSP70 mRNA. AMPK mRNA continuously increased, indicating an additional response in gene expression. We conclude that AMPK is an earlier indicator of temperature stress in rock crabs than HSP70, especially during the initial response to high temperatures. We discuss the temperature-dependent increase in AMPK activity in the context of Shelfordʼs law of tolerance. Specifically, we describe AMPK activity as a cellular marker that indicates a thermal threshold, called the pejus temperature, T p . At T p the animals leave their optimum range and enter a temperature range with a limited aerobic scope for exercise. This T p is reached periodically during annual temperature fluctuations and has higher biological significance than earlier described critical temperatures, at which the animals switch to anaerobic metabolism and HSP expression is induced.

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Section: Discussionmentioning

confidence: 97%

AMP-activated protein kinase (AMPK) in the rock crab,Cancer irroratus: an early indicator of temperature stress

Frederich

O'Rourke

Furey

et al. 2009

Journal of Experimental Biology

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“…The equilibrium constants for creatine kinase (KЈ CK ) were adjusted to the acclimation temperature and intracellular pH (Golding et al, 1995;Teague et al, 1996). Free Mg 2+ was assumed to be 1mmoll -1 (Van Waarde et al, 1990;Jibb and Richards, 2008). All data are expressed as means ± s.e.m., and were analyzed using a two-way ANOVA with subspecies and temperature as factors using Graphpad Prism (http://graphpad.com).…”

Section: Adenylatesmentioning

confidence: 99%

Intraspecific variation in the thermal plasticity of mitochondria in killifish

Dhillon

Schulte

2011

Journal of Experimental Biology

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SUMMARY Populations of the Atlantic killifish (Fundulus heteroclitus) inhabit salt marshes and estuaries along the eastern coast of NorthAmerica from Newfoundland to northern Florida, and are thus exposed to a large range of temperatures. Previous studies have shown higher whole-organism metabolic rates in the northern subspecies (F. h. macrolepidotus) compared with the southern subspecies (F. h. heteroclitus) of these fish. Here, we examine phenotypic plasticity in the response to cold temperatures between the two subspecies by acclimating fish to 5, 15 and 25°C and comparing several mitochondrial and muscle properties. The relative area of oxidative muscle versus glycolytic muscle fibers was greater in the northern subspecies at the 5 and 15°C acclimation temperatures. However, there were no differences in capillary density between the two subspecies or at different temperatures. Mitochondrial volume and surface densities increased in response to cold temperature acclimation in red and white muscle, but only in the northern killifish. Citrate synthase activities also increased in the northern killifish at 5 and 15°C. The ratio of calculated [free ADP] to [ATP] increased in the 5°C acclimated southern killifish but not in the northern killifish at 5°C when compared with the 15°C acclimation group, suggesting that there are differences in adenylate signaling for mitochondrial respiration between subspecies at low temperature. Taken together, our data indicate that the northern subspecies have a greater ability to increase mitochondrial capacity at colder temperatures compared with the southern subspecies, providing one of the few examples of intraspecific variation in phenotypic plasticity in mitochondrial amount in response to cold temperatures.

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“…AMPK activity was measured by the modified SAMS peptide [ 32 P]ATP method described by Jibb and Richards (28 (28).…”

Section: Pcr Primers Used For Identification and Quantification Of mentioning

confidence: 99%

“…These effects, which are well characterized in mammalian ischemic heart models, include lipotoxicity and uncoupling of glycolysis from glucose oxidation that exacerbates metabolic acidosis and disturbs ion homeostasis (16). Interestingly, this latter event is mediated by AMPactivated protein kinase (AMPK), which is potentially important in decreasing Ṁ O 2 and ATP demand in certain tissues in goldfish (Carassius auratus) and crucian carp during oxygen lack (28,52).…”

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confidence: 99%

Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia

Speers‐Roesch

Sandblom

Lau

et al. 2010

American Journal of Physiology-Regulatory, Integrative and Comp

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Speers-Roesch B, Sandblom E, Lau GY, Farrell AP, Richards JG. Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia. Am J Physiol Regul Integr Comp Physiol 298: R104 -R119, 2010. First published October 28, 2009 doi:10.1152/ajpregu.00418.2009.-The ability of an animal to depress ATP turnover while maintaining metabolic energy balance is important for survival during hypoxia. In the present study, we investigated the responses of cardiac energy metabolism and performance in the hypoxia-tolerant tilapia (Oreochromis hybrid sp.) during exposure to environmental hypoxia. Exposure to graded hypoxia (Ն92% to 2.5% air saturation over 3.6 Ϯ 0.2 h) followed by exposure to 5% air saturation for 8 h caused a depression of whole animal oxygen consumption rate that was accompanied by parallel decreases in heart rate, cardiac output, and cardiac power output (CPO, analogous to ATP demand of the heart). These cardiac parameters remained depressed by 50 -60% compared with normoxic values throughout the 8-h exposure. During a 24-h exposure to 5% air saturation, cardiac ATP concentration was unchanged compared with normoxia and anaerobic glycolysis contributed to ATP supply as evidenced by considerable accumulation of lactate in the heart and plasma. Reductions in the provision of aerobic substrates were apparent from a large and rapid (in Ͻ1 h) decrease in plasma nonesterified fatty acids concentration and a modest decrease in activity of pyruvate dehydrogenase. Depression of cardiac ATP demand via bradycardia and an associated decrease in CPO appears to be an integral component of hypoxia-induced metabolic rate depression in tilapia and likely contributes to hypoxic survival. fish; cardiovascular function; adenosine 5Ј-triphosphate; lipid; pyruvate dehydrogenase DURING PERIODS OF LOW OXYGEN, hypoxia-tolerant animals undergo a profound, rapid, and reversible metabolic rate depression as shown by large decreases in oxygen consumption rate (Ṁ O 2 ) and heat production (44,54). This metabolic rate depression reflects a downregulation of cellular ATP turnover to a level that can be sustained by oxygen-independent ATP production. The ability to balance ATP demand with supply and thus maintain stable cellular ATP concentration ([ATP]) is a key response ensuring hypoxic survival in tolerant animals, including many species of fishes that regularly encounter environmental hypoxia (7).A major component of the hypoxia-induced depression of ATP turnover is a reduction of cellular ATP demand, including the regulated arrest of ion pumping and anabolic pathways such as protein synthesis (30,45,49). Metabolic control analyses demonstrate, however, that ATP turnover in both active and metabolically depressed organisms can be controlled both by regulating ATP demand as well as by modulation of metabolic pathways involved in ATP supply such as mitochondrial substrate oxidation (6, 49). Our knowledge is incomplete as to how processes of ATP demand and ATP supply respond during hypoxia exposure in order to achiev...

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AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish,Carassius auratus

Cited by 108 publications

References 61 publications

AMP-activated protein kinase (AMPK) in the rock crab,Cancer irroratus: an early indicator of temperature stress

AMP-activated protein kinase (AMPK) in the rock crab,Cancer irroratus: an early indicator of temperature stress

Intraspecific variation in the thermal plasticity of mitochondria in killifish

Effects of environmental hypoxia on cardiac energy metabolism and performance in tilapia

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