Protein Turnover in Ectotherms and Its Relationships to Energetics

Houlihan, D.F.

doi:10.1007/978-3-642-75897-3_1

Cited by 175 publications

(144 citation statements)

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“…It has been suggested that the postprandial increase in O 2 consumption after feeding is a reflection of the energy cost of a surge in protein synthesis, with the total animal's O 2 consumption representing the sum of the increases in O 2 demand of the individual tissues (18). The contribution that protein synthesis makes to O 2 consumption can be calculated from the energy cost of protein synthesis.…”

Section: Discussionmentioning

confidence: 99%

“…The postprandial doubling in O 2 consumption 24 h after a meal is not generated through an increase in blood flow rate (25). In crustaceans, the microcirculation in the hepatopancreas (9), a major site of protein synthesis (18), is so well developed that these low arterial PO 2 s can be considered as quite close to the extracellular PO 2 . This tissue therefore represents an excellent opportunity to determine the O 2 sensitivity of protein synthesis in vivo.…”

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confidence: 99%

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Influence of oxygen partial pressures on protein synthesis in feeding crabs

Mente

Legeay

Houlihan

et al. 2003

American Journal of Physiology-Regulatory, Integrative and Comp

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. Influence of oxygen partial pressures on protein synthesis in feeding crabs. Am J Physiol Regul Integr Comp Physiol 284: R500-R510, 2003; 10.1152/ ajpregu.00193.2002.-Many water-breathing animals have a strategy that consists of maintaining low blood PO 2 values in a large range of water oxygenation level (4-40 kPa). This study examines the postprandial changes in O 2 consumption, arterial blood PO2, and tissue protein synthesis in the shore crab Carcinus maenas in normoxic, O2-depleted, and O2-enriched waters to study the effects of this strategy on the O2 consumption and peptide bond formation after feeding. In normoxic water (21 kPa), the arterial PO2 was 1.1 kPa before feeding and 1.2 kPa 24 h later. In water with a PO2 of 3 kPa (arterial PO2 0.6 kPa), postprandial stimulation of protein synthesis and O2 consumption were blocked. The blockade was partial at a water PO2 of 4 kPa (arterial PO2 0.8 kPa). An increase in environmental PO2 (60 kPa, arterial PO2 10 kPa) resulted in an increase in protein synthesis compared with normoxic rates. It is concluded that the arterial PO2 spontaneously set in normoxic Carcinus limits the rates of protein synthesis. The rationale for such a strategy is discussed. crustaceans; oxygen consumption; blood oxygen; hypoxia IN AIR-BREATHING HOMEOTHERMS the PO 2 in the arterial blood is regulated at 10-14 kPa in resting conditions at sea level (Ref. 6; for reference, PO 2 in air at sea level is 20-21 kPa). At the cellular level the most frequently measured values are in the 1-to 3-kPa range in the tissues (43). In numerous water breathers and other poikilotherms, the arterial PO 2 is also set at 1-3 kPa (reviewed in Ref. 27). It has been suggested that these low PO 2 values are part of a strategy of cell oxygenation termed "the low tissue O 2 strategy," which evolved with the origin of aerobic metabolism (27).In water-breathing animals, there is a strategy of gas-exchange regulation that consists of maintaining PO 2 in the arterial blood in an astonishingly low and narrow range, about 5-10 times lower than in homeotherms. Previous studies in crustaceans reported that O 2 , working in the low PO 2 range, acts 1) in a neuromodulator-like manner on the neural networks that generate the masticating and filtering movements of the foregut (5, 31) and 2) limits the oxidative metabolism of locomotor muscles (12).This paper aims to determine whether the low tissue O 2 strategy could affect protein metabolism in a water breather. Around 60 O 2 -dependent reactions exhibit values of the Michaelis-Menten constant for O 2 (K m,O 2 ) that would be rate limited at likely tissue O 2 levels (except for cytochrome-c oxidase; Ref. 43). Besides these reactions there may also be a limitation on the rate of energy supply for other processes. If these conditions are present in vivo in water breathers, we would expect that 1) an increase in tissue energy demand would result in an increase in blood PO 2 to drive an increase in tissue oxygenation and/or an increase in blood flow; 2) a reduction in envir...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Influence of oxygen partial pressures on protein synthesis in feeding crabs

Mente

Legeay

Houlihan

et al. 2003

American Journal of Physiology-Regulatory, Integrative and Comp

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“…In fish, the central site of secondary metabolism is liver, which is responsible for the synthesis and secretion of a variety of essential proteins (e.g. lipoproteins or fibrinogen), and therefore relies upon a highly active protein synthesis machinery (Houlihan, 1991) and may be most severely affected by a non-transient reduction in protein biosynthesis rates due to permanent disturbances of cellular energy metabolism.…”

Section: Inhibition Of Protein Synthesismentioning

confidence: 99%

Energy budget of hepatocytes from Antarctic fish (Pachycara brachycephalumandLepidonotothen kempi) as a function of ambient CO2: pH-dependent limitations of cellular protein biosynthesis?

Langenbuch

Pörtner

2003

Journal of Experimental Biology

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SUMMARYScenarios of rising CO2 concentration in surface waters due to atmospheric accumulation of anthropogenic CO2, or in the deep sea due to anticipated industrial dumping of CO2, suggest that hypercapnia (elevated partial pressure of CO2) will become a general stress factor in aquatic environments, with largely unknown effects on species survival and well being, especially in cold and deep waters. For an analysis of CO2 effects at the cellular level, isolated hepatocytes were prepared from two representatives of the Antarctic fish fauna, Pachycara brachycephalum and Lepidonotothen kempi. Correlated changes in energy and protein metabolism were investigated by determining the rates of oxygen consumption at various levels of PCO2, of intra- and extracellular pH, and after inhibition of protein synthesis by cycloheximide. A decrease in extracellular pH (pHe) from control levels (pHe 7.90) to pHe 6.50 caused a reduction in aerobic metabolic rate of 34-37% under both normocapnic and hypercapnic conditions. Concomitantly, protein biosynthesis was inhibited by about 80%under conditions of severe acidosis in hepatocytes from both species. A parallel drop in intracellular pH probably mediates this effect. In conclusion, the present data indicate that elevated PCO2 may limit the functional integrity of the liver due to a pronounced depression in protein anabolism. This process may contribute to the limits of whole-animal tolerance to raised CO2levels.

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“…temperature, salinity and oxygen levels) and biotic (e.g. nutritional status, size and tissue and/or organ type) factors on these processes have been summarised in several reviews over the last 20 years (Houlihan, 1991;Houlihan et al, 1995a;Houlihan et al, 1995b;Fraser and Rogers, 2007).…”

Section: Introductionmentioning

confidence: 99%

Post-prandial changes in protein synthesis in red drum (Sciaenops ocellatus) larvae

McCarthy

Fuiman

2011

Journal of Experimental Biology

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SUMMARYProtein synthesis is one of the major energy-consuming processes in all living organisms. Post-prandial changes in protein synthesis have been studied in a range of animal taxa but have been little studied in fish larvae. Using the flooding-dose method, we measured post-prandial changes in whole-body rates of protein synthesis in regularly fed red drum Sciaenops ocellatus (Linnaeus) larvae for 24-28h following their daily meal. Fractional rates of protein synthesis increased from a baseline (prefeeding) rate of 16%day -1 to a post-prandial peak of 48%day -1 ca. 8h after feeding before declining to 12%day -1 after 24-28h. The overall mean daily rate of protein synthesis was calculated as 27%day -1 . Although suggested as energetically impossible in larval poikilotherms, our results show that rates in excess of 30%day -1 can be attained by larval fishes for a few hours but are not sustained. The average daily energetic cost of protein synthesis was estimated as 34% of daily total oxygen consumption, ranging from 19% immediately before feeding to 61% during the post-prandial peak in protein synthesis. This suggests that during the post-prandial peak, protein synthesis will require a large proportion of the hourly energy production, which, given the limited metabolic scope in fish larvae, may limit the energy that could otherwise be allocated to other energy-costly functions, such as foraging and escape responses.

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Protein Turnover in Ectotherms and Its Relationships to Energetics

Cited by 175 publications

References 135 publications

Influence of oxygen partial pressures on protein synthesis in feeding crabs

Influence of oxygen partial pressures on protein synthesis in feeding crabs

Energy budget of hepatocytes from Antarctic fish (Pachycara brachycephalumandLepidonotothen kempi) as a function of ambient CO2: pH-dependent limitations of cellular protein biosynthesis?

Post-prandial changes in protein synthesis in red drum (Sciaenops ocellatus) larvae

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