Lipid composition and molecular interactions change with depth in the avian stratum corneum to regulate cutaneous water loss (original) (raw)
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Organization of lipids in avian stratum corneum: Changes with temperature and hydration
Chemistry and Physics of Lipids, 2016
In response to increases in ambient temperature (T a), many animals increase total evaporative water loss (TEWL) through their skin and respiratory passages to maintain a constant body temperature, a response that compromises water balance. In birds, cutaneous water loss (CWL) accounts for approximately 65% of TEWL at thermoneutral temperatures. Although the proportion of TEWL accounted for by CWL decreases to only 25% at high T a , the magnitude of CWL still increases, suggesting changes in the barrier function of the skin. The stratum corneum (SC) is composed of flat, dead cells called corneocytes embedded in a matrix of lipids, many of which arrange in layers called lamellae. The classes of lipids that comprise these lamellae, and their attendant physical properties, determine the rate of CWL. We measured CWL at 25, 30, 35, and 40 C in House Sparrows (Passer domesticus) caught in the winter and summer, and in sparrows acclimated to warm and cold lab environments. We then used Fourier transform infrared spectroscopy to measure lipid-lipid and lipid-water interactions in the SC under different conditions of temperature and hydration, and correlated these results with lipid classes in the SC. As CWL increased at higher temperatures, the amount of gauche defects in lipid alkyl chains increased, indicating that lipid disorder is partially responsible for higher CWL at high temperatures. However, variation in CWL between groups could not be explained by the amount of gauche defects, and this remaining variation may be attributed to greater amounts of cerebrosides in birds with low CWL, as the sugar moieties of cerebrosides lie outside lipid lamellae and form strong hydrogen bonds with water molecules. 2015 Elsevier Ireland Ltd. All rights reserved.
Lipid composition of the stratum corneum and cutaneous water loss in birds along an aridity gradient
The Journal of experimental biology, 2012
Intercellular and covalently bound lipids within the stratum corneum (SC), the outermost layer of the epidermis, are the primary barrier to cutaneous water loss (CWL) in birds. We compared CWL and intercellular SC lipid composition in 20 species of birds from desert and mesic environments. Furthermore, we compared covalently bound lipids with CWL and intercellular lipids in the lark family (Alaudidae). We found that CWL increases in birds from more mesic environments, and this increase was related to changes in intercellular SC lipid composition. The most consistent pattern that emerged was a decrease in the relative amount of cerebrosides as CWL increased, a pattern that is counterintuitive based on studies of mammals with Gaucher disease. Although covalently bound lipids in larks did not correlate with CWL, we found that covalently bound cerebrosides correlated positively with intercellular cerebrosides and intercellular cholesterol ester, and intercellular cerebrosides correlated...
Presence and persistence of a highly ordered lipid phase state in the avian stratum corneum
The Journal of experimental biology, 2018
To survive high temperatures in a terrestrial environment, animals must effectively balance evaporative heat loss and water conservation. In passerine birds, cutaneous water loss (CWL) is the primary avenue of water loss at thermoneutral temperatures, and increases slightly as ambient temperature increases, indicating a change in the permeability of the skin. In the stratum corneum (SC), the outermost layer of skin, lipids arranged in layers called lamellae serve as the primary barrier to CWL in birds. The permeability of these lamellae depends in large part on the ability of lipid molecules to pack closely together in an ordered orthorhombic phase state. However, as temperature increases, lipids of the SC become more disordered, and may pack in more permeable hexagonal or liquid crystalline phase states. In this study, we used Fourier transform infrared spectroscopy to monitor the phase state of lipids in the SC of house sparrows () at skin temperatures ranging from 25 to 50°C. As ...
Journal of Experimental …, 2008
Because cutaneous water loss (CWL) represents half of total water loss in birds, selection to reduce CWL may be strong in desert birds. We previously found that CWL of house sparrows from a desert population was about 25% lower than that of individuals from a mesic environment. The stratum corneum (SC), the outer layer of the epidermis, serves as the primary barrier to water vapor diffusion through the skin. The avian SC is formed by layers of corneocytes embedded in a lipid matrix consisting of cholesterol, free fatty acids and two classes of sphingolipids, ceramides and cerebrosides. The SC of birds also serves a thermoregulatory function; high rates of CWL keep body temperatures under lethal limits in episodes of heat stress.
Journal of …, 2008
Because cutaneous water loss (CWL) represents half of total water loss in birds, selection to reduce CWL may be strong in desert birds. We previously found that CWL of house sparrows from a desert population was about 25% lower than that of individuals from a mesic environment. The stratum corneum (SC), the outer layer of the epidermis, serves as the primary barrier to water vapor diffusion through the skin. The avian SC is formed by layers of corneocytes embedded in a lipid matrix consisting of cholesterol, free fatty acids and two classes of sphingolipids, ceramides and cerebrosides. The SC of birds also serves a thermoregulatory function; high rates of CWL keep body temperatures under lethal limits in episodes of heat stress.
Chemistry and physics of lipids, 2017
The outermost layer of skin, the stratum corneum (SC), contains a complex mixture of lipids, which controls the rate of cutaneous water loss (CWL) in reptiles, mammals, and birds. However, the molecular structure of SC lipids and how molecular configurations influence CWL is poorly understood. Here, the organization and structure of SC lipids extracted from birds were investigated by means of Langmuir films. Properties of lipids from the SC of arid and semi-arid adapted larks, known to have a low CWL, were compared with lipids extracted from the SC of mesic lark species with higher CWL to gain insight into how structure impacts CWL. Film properties were probed with surface pressure-area isotherms, Brewster angle microscopy (BAM), and vibrational sum frequency generation (VSFG). Results indicate organization and ordering of SC lipids in the arid-adapted hoopoe lark was vastly different from all other species, forming a miscible, rigid monolayer, whereas monolayers from semi-arid and ...
Avian Epidermal Lipids: Functional Considerations and Relationship to Feathering1
American Zoologist, 2000
The avian epidermis is composed of unique sebokeratinocytes that elaborate and secrete sebum-like lipids as they cornify. In addition to the lipid droplets, the avian epidermis elaborates, but rarely secretes, lipid-enriched organelles, the multigranular bodies. The multigranular bodies are analogous to the lamellar bodies of mammals (Menon et al., 1991), the secretion of which results in formation of occlusive lipid bilayers characteristic of mammalian stratum corneum and providing the permeability barrier. However, in contrast to mammals, the avian multigranular bodies form the reserve barrier mechanism. In the basal state, when multigranular bodies are not secreted, the avian cutaneous barrier is deficient, but allows evaporative cooling for thermoregulation. However, under conditions of water deficit, multigranular body secretion allows for rapid facultative waterproofing, as shown in zebra finches (Taenyopygia guttata). In certain glabrous regions of the skin, such as the maxillary rictus, interdigital web, and combs and wattles in the domestic fowl, there is a high degree of epidermal lipid secretion. Also specialized feathers such as powder downs elaborate lipid rich material, which can be classified as secretion. Additionally, an inverse relation between epidermal lipogenesis and the degree of feathering has been demonstrated, as in temporarily bare areas (e.g., brood patches) and following permanent feather loss from the head accompanying attainment of maturity in certain ibises and storks. In the latter, the neo-apteria often hold large reserves of carotenoids dissolved in the lipid droplets, possibly related to an altered gradient of retinoids influencing feather morphogenesis. Unusual secondary functions of epidermal lipids include cosmetic coloration (e.g., in the Japanese Crested Ibis) and chemical defense (e.g., in the Pitohui).
Skin lipids from Saudi Arabian birds
Saudi Journal of Biological Sciences, 2014
Skin lipids play an important role in the regulation of cutaneous water loss (CWL). Earlier studies have shown that Saudi desert birds exhibit a tendency of reduced CWL than birds from temperate environment due to adaptive changes in composition of their skin lipids. In this study, we used thin-layer chromatography (TLC) for separation and detection of nonpolar and polar lipids from the skin of six bird species including sooty gull, brown booby, house sparrow, Arabian waxbill, sand partridge, and laughing dove. The lipids were separated and detected on Silica gel G coated TLC plates and quantified by using densitometric image analysis. Rf values of the non-polar lipids were as follows: cholesterol (0.29), free fatty acids (0.58), triacylglycerol (0.69), fatty acids methyl esters (0.84) and cholesterol ester (0.97). Rf values for the polar lipids were: cerebroside (0.42), ceramide (0.55) and cholesterol (0.73). The results showed the abundance of fatty acids methyl esters (47.75-60.46%) followed by triacylglycerol (12.69-24.14%). The remaining lipid compositions were as follows: cholesterol (4.09-13.18%), ceramide (2.18-13.27%), and cerebroside (2.53-12.81%). In conclusion, our findings showed that TLC is a simple and sensitive method for the separation and quantification of skin lipids. We also reported a new protocol for lipid extraction using the zirconia beads for efficient disruption of skin tissues. This study will help us better understand the role of skin lipids in adaptive physiology towards adverse climatic conditions.
Proceedings of the Royal Society B: Biological Sciences, 2016
The water vapour permeability barrier of mammals and birds resides in the stratum corneum (SC), the outermost layer of the epidermis. The molar ratio and molecular arrangement of lipid classes in the SC determine the integrity of this barrier. Increased chain length and polarity of ceramides, the most abundant lipid class in mammalian SC, contribute to tighter packing and thus to reduced cutaneous evaporative water loss (CEWL). However, tighter lipid packing also causes low SC hydration, making it brittle, whereas high hydration softens the skin at the cost of increasing CEWL. Cerebrosides are not present in the mammalian SC; their pathological accumulation occurs in Gaucher's disease, which leads to a dramatic increase in CEWL. However, cerebrosides occur normally in the SC of birds. We tested the hypothesis that cerebrosides are also present in the SC of bats, because they are probably necessary to confer pliability to the skin, a quality needed for flight. We examined the SC ...
Climate change and cutaneous water loss of birds
Journal of Experimental Biology, 2012
Summary There is a crucial need to understand how physiological systems of animals will respond to increases in global air temperature. Water conservation may become more important for some species of birds, especially those living in deserts. Lipids of the stratum corneum (SC), the outer layer of the epidermis, create the barrier to water vapor diffusion, and thus control cutaneous water loss (CWL). An appreciation of the ability of birds to change CWL by altering lipids of the skin will be important to predict responses of birds to global warming. The interactions of these lipids are fundamental to the modulation of water loss through skin. Cerebrosides, with their hexose sugar moiety, are a key component of the SC in birds, but how these lipids interact with other lipids of the SC, or how they form hydrogen bonds with water molecules, to form a barrier to water vapor diffusion remains unknown. An understanding of how cerebrosides interact with other lipids of the SC, and of how t...