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      Comparative Physiology of Energy Metabolism: Fishing for Endocrine Signals in the Early Vertebrate Pool


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          Energy is the common currency of life. To guarantee a homeostatic supply of energy, multiple neuro-endocrine systems have evolved in vertebrates; systems that regulate food intake, metabolism, and distribution of energy. Even subtle (lasting) dysregulation of the delicate balance of energy intake and expenditure may result in severe pathologies. Feeding-related pathologies have fueled research on mammals, including of course the human species. The mechanisms regulating food intake and body mass are well-characterized in these vertebrates. The majority of animal life is ectothermic, only birds and mammals are endotherms. What can we learn from a (comparative) study on energy homeostasis in teleostean fishes, ectotherms, with a very different energy budget and expenditure? We present several adaptation strategies in fish. In recent years, the components that regulate food intake in fishes have been identified. Although there is homology of the major genetic machinery with mammals (i.e., there is a vertebrate blueprint), in many cases this does not imply analogy. Although both mammals and fish must gain their energy from food, the expenditure of the energy obtained is different. Mammals need to spend vast amounts of energy to maintain body temperature; fishes seem to utilize a broader metabolic range to their advantage. In this review, we briefly discuss ecto- and endothermy and their consequences for energy balance. Next, we argue that the evolution of endothermy and its (dis-)advantages may explain very different strategies in endocrine regulation of energy homeostasis among vertebrates. We follow a comparative and evolutionary line of thought: we discuss similarities and differences between fish and mammals. Moreover, given the extraordinary radiation of teleostean fishes (with an estimated number of 33,400 contemporary species, or over 50% of vertebrate life forms), we also compare strategies in energy homeostasis between teleostean species. We present recent developments in the field of (neuro)endocrine regulation of energy balance in teleosts, with a focus on leptin.

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          A cause-and-effect understanding of climate influences on ecosystems requires evaluation of thermal limits of member species and of their ability to cope with changing temperatures. Laboratory data available for marine fish and invertebrates from various climatic regions led to the hypothesis that, as a unifying principle, a mismatch between the demand for oxygen and the capacity of oxygen supply to tissues is the first mechanism to restrict whole-animal tolerance to thermal extremes. We show in the eelpout, Zoarces viviparus, a bioindicator fish species for environmental monitoring from North and Baltic Seas (Helcom), that thermally limited oxygen delivery closely matches environmental temperatures beyond which growth performance and abundance decrease. Decrements in aerobic performance in warming seas will thus be the first process to cause extinction or relocation to cooler waters.
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            A new compilation of fossil data on invertebrate and vertebrate families indicates that four mass extinctions in the marine realm are statistically distinct from background extinction levels. These four occurred late in the Ordovician, Permian, Triassic, and Cretaceous periods. A fifth extinction event in the Devonian stands out from the background but is not statistically significant in these data. Background extinction rates appear to have declined since Cambrian time, which is consistent with the prediction that optimization of fitness should increase through evolutionary time.
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              Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression.

              Nutritional deprivation suppresses immune function. The cloning of the obese gene and identification of its protein product leptin has provided fundamental insight into the hypothalamic regulation of body weight. Circulating levels of this adipocyte-derived hormone are proportional to fat mass but maybe lowered rapidly by fasting or increased by inflammatory mediators. The impaired T-cell immunity of mice now known to be defective in leptin (ob/ob) or its receptor (db/db), has never been explained. Impaired cell-mediated immunity and reduced levels of leptin are both features of low body weight in humans. Indeed, malnutrition predisposes to death from infectious diseases. We report here that leptin has a specific effect on T-lymphocyte responses, differentially regulating the proliferation of naive and memory T cells. Leptin increased Th1 and suppressed Th2 cytokine production. Administration of leptin to mice reversed the immunosuppressive effects of acute starvation. Our findings suggest a new role for leptin in linking nutritional status to cognate cellular immune function, and provide a molecular mechanism to account for the immune dysfunction observed in starvation.

                Author and article information

                Front Endocrinol (Lausanne)
                Front Endocrinol (Lausanne)
                Front. Endocrinol.
                Frontiers in Endocrinology
                Frontiers Media S.A.
                02 March 2017
                : 8
                [1] 1Department of Animal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University , Nijmegen, Netherlands
                Author notes

                Edited by: Maximilian Michel, University of Michigan, USA

                Reviewed by: Thomas W. Moon, University of Ottawa, Canada; Sergio Polakof, French National Institute for Agricultural Research (INRA), France; Richard Londraville, University of Akron, USA

                *Correspondence: Gert Flik, g.flik@ 123456science.ru.nl

                Specialty section: This article was submitted to Experimental Endocrinology, a section of the journal Frontiers in Endocrinology

                Copyright © 2017 van de Pol, Flik and Gorissen.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                : 01 December 2016
                : 10 February 2017
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 213, Pages: 18, Words: 16636

                Endocrinology & Diabetes
                leptin,insulin,gills,metabolism,aerobic scope,oxygen,teleost,fish
                Endocrinology & Diabetes
                leptin, insulin, gills, metabolism, aerobic scope, oxygen, teleost, fish


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