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Metabolic and Kidney Diseases in the Setting of Climate Change, Water Shortage, and Survival Factors

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Metabolic and Kidney Diseases in the Setting of Climate Change, Water Shortage, and Survival Factors SPECIAL ARTICLE www.jasn.org Metabolic and Kidney Diseases in the Setting of Climate Change, Water Shortage, and Survival Factors † Richard J. Johnson,* Peter Stenvinkel, Thomas Jensen,* Miguel A. Lanaspa,* Carlos Roncal,* ‡ Zhilin Song,* Lise Bankir, and Laura G. Sánchez-Lozada§ *Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado; †Division of Renal Medicine, Department of Clinical Science Intervention and Technology, Karolinska University Hospital, Stockholm, Sweden; ‡Institut National de las Santé et de la Recherche Medicalé UMRS 1138, Centre de Recherche des Cordeliers, Paris, France; and §Laboratory of Renal Physiopathology, Instituto Nacional de Cardiologia Ignacio Chávez, Mexico City, Mexico ABSTRACT Climate change (global warming) is leading to an increase in heat extremes and epidemics and their relationship to local coupled with increasing water shortage, provides a perfect storm for a new era of temperatures and changing climate, space environmental crises and potentially, new diseases. We use a comparative physio- constraints prevented it from being able to logic approach to show that one of the primary mechanisms by which animals address a more central question on the bi- protect themselves against water shortage is to increase fat mass as a means for ology of water conservation and how it re- providing metabolic water. Strong evidence suggests that certain hormones lates to disease. Here we review how various (vasopressin), foods (fructose), and metabolic products (uric acid) function as species protect themselves from dehydra- survival signals to help reduce water loss and store fat (which also provides a source tion, and we identify nutrient, hormonal of metabolic water). These mechanisms are intricately linked with each other and and metabolic pathways triggered by hy- stimulated by dehydration and hyperosmolarity. Although these mechanisms were perosmolarity that link water conservation protective in the setting of low sugar and low salt intake in our past, today, the combination of diets high in fructose and salty foods, increasing temperatures, and with survival. We also discuss how these decreasing available water places these survival signals in overdrive and may be pathways may predict diseases that will accelerating the obesity and diabetes epidemics. The recent discovery of multiple dominate the next millennium. Impor- epidemics of CKD occurring in agricultural workers in hot and humid environments tantly, climate change, heat stress, and may represent harbingers of the detrimental consequences of the combination of water shortage not only will affect kidney climate change and overactivation of survival pathways. disease, but risk for metabolic diseases in- cluding obesity and diabetes. J Am Soc Nephrol 27: 2247–2256, 2016. doi: 10.1681/ASN.2015121314 HOW ANIMALS SURVIVE WATER The 21st century is bringing new chal- moderate water shortage (i.e.,1.0–1.7 m3 SHORTAGE lenges with population expansion, a de- water per person per year), and 10% have crease in natural resources, and climate extreme water shortage (defined as The transition of vertebrates from sea based change. Mean temperatures increased by ,0.5 m3 per person per year), with the pri- to land was associated with many adapta- 0.8°C since 1880, with two thirds of the mary areas affected being Africa, southern tions, but some of the most important were change occurring since 1975, and they and eastern Asia, and the Middle East.4 mechanisms to conserve water, including are projected to increase by 3°C to 4°C Increasing water shortage coupled by the end of the 21st century.1,2 Temper- with climate change increases the risk Published online ahead of print. Publication date atureextremeshavealsoincreasedby75% for dehydration-associated diseases. For available at www.jasn.org. because of climate change.3 Continued example, there is increasing evidence that Correspondence: Dr. Richard J. Johnson, Division population growth and to a lesser extent, climate change may have a role in epi- of Renal Diseases and Hypertension, University of Colorado Denver, 12700 East 19th Avenue, Aurora climate change have also resulted in de- demics of CKD that are occurring among CO 80045. Email: [email protected] 4,5 6 creasing water resources. Today, one workers in hot environments. While this Copyright © 2016 by the American Society of half of the world population suffer latter paper focuses on the sites of these Nephrology J Am Soc Nephrol 27: 2247–2256, 2016 ISSN : 1046-6673/2708-2247 2247 SPECIAL ARTICLE www.jasn.org ways to store water, minimize water loss, Although ureotelic animals have ob- but when fat is oxidized, water and car- and generate water.7 ligate water loss to help excrete metabolic bon dioxide are released. For every gram wastes, urinary loss is minimized by of fat metabolized, 1.12 ml water is gen- Water Storage urinary concentration, a process largely erated.16 Liver or muscle glycogen also Some terrestrial animals store water in driven by vasopressin (or vasotocin in generates 0.6 ml water per gram of gly- their bladders. The water-holding frog lower vertebrates). Vasopressin reduces cogen metabolized.17 Because glycogen (Cyclorana platycephala)oftheSandy water excretion by allowing water reab- is water soluble, it also releases potas- Desert of Australia, for example, stores sorption in the collecting ducts, but it also sium and water during metabolism, ac- so much water that it may double its increases sodium and urea reabsorption. counting for an additional 3 ml water per weight.8 These frogs were a favorite The reduction in urea excretion by vaso- gram of glycogen metabolized.18,19 The source of water for the Tiwi people dur- pressin improves urinary concentration marked diuresis after initiation of a low- ing hot summers. Some frogs live 5 years by increasingureaaccumulationintherenal carbohydrate diet is partially because without drinking water, which is because medulla, which aids water reabsorption. of water released during glycogen me- they utilize water stored in their bladders tabolism.19 Although glycogen metabo- and also generate water during the me- Reducing Nonrenal Water Loss lism produces metabolic water, most tabolism of fat.7,8 The giant tortoise of Water loss also occurs through the skin organisms store more fat than glycogen. the Galapagos Islands stores water in and lungs, where it helps regulate body Thus, fat is the major source of metabolic their urinary bladder. After rain, the tor- temperature when animals are exposed water for most animals. toise voids their bladder urine (which to heat. A lack of sweating can result in a Metabolic water is used by many contains urea and other waste products) marked rise in body temperature and animals to survive periods of water and drinks copiously to refill their blad- circulatory collapse (heat shock). In shortage. Marine whales obtain much der with fresh water. When needed, the contrast, excessive sweating without re- of their water from the burning of fat.20 turtle reabsorbs the water through the hydration may result in hypernatremia Although capable of ingesting seawater bladder wall, while at the same time, ex- and volume depletion. and excreting a urine more concentrated creting some of its wastes into it, and Desert rodents minimize water loss by than seawater, whales rarely use this over time, the osmolarity of the bladder hiding during the day in burrows, where method for obtaining water.20 Lungfish urine increases.9 temperatures are lower and humidity is obtain water from fat metabolism while high. Lungfish coat themselves with they estivate in the mud for 1–2 years. Reduced Urinary Water Losses slime to minimize water loss as they Desert rodents, such as the sand rat Homer Smith6 proposed that the evolu- burrow and estivate in the mud. Estivat- (Psammomys obesus), have high body tion from aquatic to terrestrial environ- ing frogs (C. platycephala) form cocoons fat, which they use to generate water ments required efficient ways to excrete from sloughed epithelial layers of skin.11 during times of need. Larger desert animals, nitrogen to help minimize loss of wa- Tree frogs decrease water loss by secret- such as the camel and oryx, also use meta- ter.10 Most aquatic animals excrete am- ing an impermeable waxy material onto bolic water, and in the oryx, this may ac- monia, the simplest nitrogen product, as their skin.11 Lemurs estivate in tree hol- count for 24% of its overall water needs.21 their means for eliminating nitrogen lows to avoid sun exposure and reduce Some obligatory water loss by the waste products (ammoniotely). In con- their metabolism and water needs. The lung occurs during fat metabolism be- trast, ammonia is not an appropriate dromedary camel conserves water by cause ofthe need to excrete carbondioxide compound for nitrogen excretion by ter- minimizing sweating because of a reduc- that may counter the gain of water pro- restrial animals, because its renal excre- tion in sweat glands. The camel also does vided during fat metabolism.22 However, tion requires 400 ml water per 1 gram not pant and has adaptations in its nose animals like camels have developed tech- ammonia and blood levels .0.05 mM that minimize respiratory losses of wa- niques to reduce water loss from their air- are neurotoxic.10 Rather, urea excretion ter.12,13 The consequence is significant ways and skin.12,13 is common among land amphibians and diurnal variation in body temperature mammals, because it is concentrated (as much as 6°C),
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