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Exogenous Lipids Influence Permeability Barrier Recovery in Acetone-Treated Murine Skin

Exogenous Lipids Influence Permeability Barrier Recovery in Acetone-Treated Murine Skin Abstract • Background and Design.— When the epidermal permeability barrier is perturbed with acetone, transcutaneous water loss returns to normal over 24 hours in parallel with the reappearance of stratum corneum lipids, derived from secreted lamellar bodies and accelerated lipid synthesis. Prior studies have demonstrated a separate requirement for cholesterol, fatty acid, and ceramide synthesis for barrier homeostasis, but the requirement for these lipids individually or together for barrier function is not known. We therefore applied these lipids alone or in various mixtures to acetonetreated hairless mouse skin and assessed barrier recovery. Results.— Ceramide and fatty acid alone, and their complex derivatives (cholesterol esters and cerebrosides), and two-component mixtures of fatty acid plus ceramide, cholesterol plus fatty acid, or cholesterol plus ceramide delayed barrier recovery. In contrast, complete mixtures of ceramide, fatty acid, and cholesterol allowed normal barrier recovery. Moreover, fluorescent-labeled cholesterol, fatty acid, and ceramide rapidly traversed the stratum corneum with uptake into the epidermal nucleated layers. Finally, incomplete, but not complete mixtures produce abnormal lamellar bodies, leading to abnormal stratum corneum intercellular membrane bilayers. Conclusions.— (1) Topical applications of individual lipids or incomplete mixtures of lipids interfere with barrier Conclusions.—(1) ery, while complete mixtures of cholesterol, fatty acid, and ceramide allow normal barrier repair; and (2) incomplete mixtures of topical lipids appear to inhibit barrier recovery at the level of the lamellar body resulting in abnormal intercellular membrane structures in the stratum corneum, abnormalities that do not occur when a complete lipid mixture is provided.(Arch Dermatol. 1993;129:728-738) References 1. Elias PM, Menon GK. Structural and lipid biochemical correlates of the epidermal permeability barrier . Adv Lipid Res. 1991;24: 1-26. 2. Yardley HJ, Summerly R. Lipid composition and metabolism in normal and diseased epidermis . Pharmacol Ther. 1981;13:357-383.Crossref 3. Landmann L. The epidermal permeability barrier . Anat Embryol. 1988;178:1-13.Crossref 4. Abe Ohkido M, Abe T, Matsuo I. Epidermal cholesterol as a barrier for transepidermal water loss . In: Seiji M, Bernstein IA, eds. Biochemistry of Cutaneous Epidermal Differentiation . Tokyo, Japan: University of Tokyo Press; 1977:230-239. 5. Menon GK, Feingold KR, Moser AH, et al. De novo sterologenesis in the skin, II: regulation by cutaneous barrier requirements . J Lipid Res. 1985;26:418-427. 6. Grubauer G, Feingold KR, Elias PM. Relationship of epidermal lipogenesis to cutaneous barrier function . J Lipid Res. 1987;28:746-752. 7. Proksch E, Elias PM, Feingold KR. Regulation of 3-hydroxy-3methylglutaryl-coenzyme A reductase activity in murine epidermis: modulation of enzyme content and activation state by barrier requirements . J Clin Invest. 1990;85:874-882.Crossref 8. Feingold KR, Brown BE, Lear SR, Moser AH, Elias PM. Effect of essential fatty acid deficiency on cutaneous sterol synthesis . J Invest Dermatol. 1986;87:588-591.Crossref 9. Feingold KR, Man MQ, Menon GK, Cho SS, Brown BE, Elias PM. Cholesterol synthesis is required for cutaneous barrier function in mice . J Clin Invest. 1990;86:1738-1745.Crossref 10. Feingold KR, Man MQ, Proksch E, Menon GK, Brown BE, Elias PM. The lovastatin-treated rodent: a new model of barrier disruption and epidermal hyperplasia . J Invest Dermatol. 1991;96:201-209.Crossref 11. Prottey C. Essential fatty acids and the skin . Br J Dermatol. 1976;94:579-587.Crossref 12. Elias PM, Brown B, Ziboh VA. The permeability barrier in essential fatty acid deficiency: evidence for a direct role for linoleic acid in epidermal barrier function . J Invest Dermatol. 1980;74:230-233.Crossref 13. Houtsmuller VMT, Van der Beck A. Effects of topical applications of fatty acids in essential fatty acid deficiency . Progr Lipid Res. 1981;20:219-224.Crossref 14. Holleran WM, Feingold KR, Man MQ, Gao WN, Lee JM, Elias PM. Regulation of epidermal sphingolipid synthesis by permeability barrier function . J Lipid Res. 1991;32:1151-1158. 15. Holleran WM, Man MQ, Menon GK, Elias PM, Feingold KR. Sphingolipids are required for mammalian barrier function, II: inhibition of sphingolipid synthesis delays barrier recovery after acute perturbation . J Clin Invest. 1991;88:1338-1345.Crossref 16. Yeagle PL. Lipid regulation of cell membrane structure and function . FASEB J. 1989;3:1833-1842. 17. Spector AA, Yorek MA. Membrane lipid composition and cellular function . J Lipid Res. 1985;26:1015-1035. 18. Abrahamsson S, Dahlen B, Lofgren H, Pascher I, Sundell S. Molecular arrangement and confirmation of lipids of relevance to membrane structure . In: Abrahamsson S, ed. Structure of Biological Membranes . 1977:1-23. 19. Cullis PR, Hope MJ. Physical properties and functional roles of lipids in membranes . In: Vance DE, Vance JE, eds. Biochemistry of Lipids and Membranes . Menlo Park, Calif: The Benjamin Cummings Publishing Co Inc; 1985:25-72. 20. Hou SYE, Mitra AK, White SH, Menon GK, Ghadially R, Elias PM. Membrane structures in normal and essential fatty acid deficient stratum corneum: characterization by ruthenium tetroxide staining and x-ray diffraction . J Invest Dermatol. 1991;96:215-223.Crossref 21. Abraham W, Downing DT. Preparation of model membranes for skin permeability studies using stratum corneum lipids . J Invest Dermatol. 1989;93:809-813.Crossref 22. Wertz PW, Abraham W, Landmann L, Downing DT. Preparation of liposomes from stratum corneum lipids . J Invest Dermatol. 1986;87:582-584.Crossref 23. Lampe MA, Burlingame AL, Whitney J, et al. Human stratum corneum lipids: characterization and regional variations . J Lipid Res. 1983;24:120-130. 24. Menon GK, Grayson S, Brown BE, Elias PM. Lipokeratinocytes of the epidermis of a cetacean (Phocena phocena): histochemistry, ultrastructure, and lipid composition . Cell Tissue Res. 1986; 244:385-394.Crossref 25. Squier CA, Cox P, Wertz PW. Lipid content and water permeability of skin and oral mucosa . J Invest Dermatol. 1991;96: 123-126.Crossref 26. Grubauer G, Feingold KR, Elias PM. Lipid content and lipid type as determinants of the epidermal permeability barrier . J Lipid Res. 1989;30:89-96. 27. Imokawa G, Akasaki S, Hattori M, Yoshizuka N. Selective recovery of deranged water-holding properties by stratum corneum lipids . J Invest Dermatol . 1986;87:758-761.Crossref 28. Imokawa G, Akasaki S, Minematsu, Y, Kawai M. Importance of intercellular lipids in water-retention properties of the stratum corneum: induction and recovery study of surfactant dry skin . Arch Dermatol Res. 1989;281:45-51.Crossref 29. Ghadially RG, Halkier-Sorensen L, Elias PM. The effects of petrolatum on stratum corneum structure and function . J Am Acad Dermatol. 1992;26:387-396.Crossref 30. Elias PM, Williams ML. Neutral lipid storage disease with ichthyosis: defective lamellar body contents and intercellular dispersion . Arch Dermatol. 1985;121:1000-1008.Crossref 31. Koone MD, Rizzo WB, Elias PM, Williams ML, Lightner V, Pinnell SR. Ichthyosis, mental retardation, and asymptomatic spasticity: a new neurocutaneous syndrome with normal fatty alcohol: NAD+ oxidoreductase activity . Arch Dermatol. 1990;126:1485-1490.Crossref 32. Menon GK, Feingold KR, Man MQ, Schaude M, Elias PM. Structural basis for the barrier abnormality following inhibition of HMG CoA reductase in murine epidermis . J Invest Dermatol. 1992; 98:209-219.Crossref 33. Elias PM, Williams ML, Maloney ME, et al. Stratum corneum lipids in disorders of cornification: steroid sulfatase and cholesterol sulfate in normal desquamation and the pathogenesis of recessive X-linked ichthyosis . J Clin Invest. 1984;74:1414-1421.Crossref 34. Freinkel RK, Traczyk TN. Acid hydrolases of the epidermis: subcellular localization and relationship to cornification . J Invest Dermatol. 1985;80:441-446.Crossref 35. Menon GK, Grayson S, Elias PM. Cytochemical and biochemical localization of lipase and sphingomyelinase activity in mammalian epidermis . J Invest Dermatol. 1986;86:591-597.Crossref 36. Elias PM, Menon GK, Grayson S, Brown BE. Membrane structural alterations in murine stratum corneum: relationship to the localization of polar lipids and phospholipases . J Invest Dermatol. 1988;91:3-10.Crossref 37. Bergers M, Verhagen DR, Jongerius M, Van der Kerkhof PCM, Mier PD. A unique phospholipase A2 in human epidermis: its physiological functions and its level in certain dermatoses . J Invest Dermatol. 1988;90:23-25.Crossref 38. Hansen HS, Jensen B. Essential function of linoleic acid esterified in acylglycosylceramide and acylceramide in maintaining the epidermal water permeability barrier: evidence from feeding studies with linoleate, oleate, arachidonate, columbinate, and alphalinolenate . Biochim Biophys Acta . 1985;834:357-363.Crossref 39. Elliott WJ, Huo ZY, Meyer PE, Echols BS, Forats T. Dose-response and time-course of distribution of columbinic acid in rat skin . FASEB J. 1988;2:A1064. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Dermatology American Medical Association

Exogenous Lipids Influence Permeability Barrier Recovery in Acetone-Treated Murine Skin

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American Medical Association
Copyright
Copyright © 1993 American Medical Association. All Rights Reserved.
ISSN
0003-987X
eISSN
1538-3652
DOI
10.1001/archderm.1993.01680270066008
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Abstract

Abstract • Background and Design.— When the epidermal permeability barrier is perturbed with acetone, transcutaneous water loss returns to normal over 24 hours in parallel with the reappearance of stratum corneum lipids, derived from secreted lamellar bodies and accelerated lipid synthesis. Prior studies have demonstrated a separate requirement for cholesterol, fatty acid, and ceramide synthesis for barrier homeostasis, but the requirement for these lipids individually or together for barrier function is not known. We therefore applied these lipids alone or in various mixtures to acetonetreated hairless mouse skin and assessed barrier recovery. Results.— Ceramide and fatty acid alone, and their complex derivatives (cholesterol esters and cerebrosides), and two-component mixtures of fatty acid plus ceramide, cholesterol plus fatty acid, or cholesterol plus ceramide delayed barrier recovery. In contrast, complete mixtures of ceramide, fatty acid, and cholesterol allowed normal barrier recovery. Moreover, fluorescent-labeled cholesterol, fatty acid, and ceramide rapidly traversed the stratum corneum with uptake into the epidermal nucleated layers. Finally, incomplete, but not complete mixtures produce abnormal lamellar bodies, leading to abnormal stratum corneum intercellular membrane bilayers. Conclusions.— (1) Topical applications of individual lipids or incomplete mixtures of lipids interfere with barrier Conclusions.—(1) ery, while complete mixtures of cholesterol, fatty acid, and ceramide allow normal barrier repair; and (2) incomplete mixtures of topical lipids appear to inhibit barrier recovery at the level of the lamellar body resulting in abnormal intercellular membrane structures in the stratum corneum, abnormalities that do not occur when a complete lipid mixture is provided.(Arch Dermatol. 1993;129:728-738) References 1. Elias PM, Menon GK. Structural and lipid biochemical correlates of the epidermal permeability barrier . Adv Lipid Res. 1991;24: 1-26. 2. Yardley HJ, Summerly R. Lipid composition and metabolism in normal and diseased epidermis . Pharmacol Ther. 1981;13:357-383.Crossref 3. Landmann L. The epidermal permeability barrier . Anat Embryol. 1988;178:1-13.Crossref 4. Abe Ohkido M, Abe T, Matsuo I. Epidermal cholesterol as a barrier for transepidermal water loss . In: Seiji M, Bernstein IA, eds. Biochemistry of Cutaneous Epidermal Differentiation . Tokyo, Japan: University of Tokyo Press; 1977:230-239. 5. Menon GK, Feingold KR, Moser AH, et al. De novo sterologenesis in the skin, II: regulation by cutaneous barrier requirements . J Lipid Res. 1985;26:418-427. 6. Grubauer G, Feingold KR, Elias PM. Relationship of epidermal lipogenesis to cutaneous barrier function . J Lipid Res. 1987;28:746-752. 7. Proksch E, Elias PM, Feingold KR. Regulation of 3-hydroxy-3methylglutaryl-coenzyme A reductase activity in murine epidermis: modulation of enzyme content and activation state by barrier requirements . J Clin Invest. 1990;85:874-882.Crossref 8. Feingold KR, Brown BE, Lear SR, Moser AH, Elias PM. Effect of essential fatty acid deficiency on cutaneous sterol synthesis . J Invest Dermatol. 1986;87:588-591.Crossref 9. Feingold KR, Man MQ, Menon GK, Cho SS, Brown BE, Elias PM. Cholesterol synthesis is required for cutaneous barrier function in mice . J Clin Invest. 1990;86:1738-1745.Crossref 10. Feingold KR, Man MQ, Proksch E, Menon GK, Brown BE, Elias PM. The lovastatin-treated rodent: a new model of barrier disruption and epidermal hyperplasia . J Invest Dermatol. 1991;96:201-209.Crossref 11. Prottey C. Essential fatty acids and the skin . Br J Dermatol. 1976;94:579-587.Crossref 12. Elias PM, Brown B, Ziboh VA. The permeability barrier in essential fatty acid deficiency: evidence for a direct role for linoleic acid in epidermal barrier function . J Invest Dermatol. 1980;74:230-233.Crossref 13. Houtsmuller VMT, Van der Beck A. Effects of topical applications of fatty acids in essential fatty acid deficiency . Progr Lipid Res. 1981;20:219-224.Crossref 14. Holleran WM, Feingold KR, Man MQ, Gao WN, Lee JM, Elias PM. Regulation of epidermal sphingolipid synthesis by permeability barrier function . J Lipid Res. 1991;32:1151-1158. 15. Holleran WM, Man MQ, Menon GK, Elias PM, Feingold KR. Sphingolipids are required for mammalian barrier function, II: inhibition of sphingolipid synthesis delays barrier recovery after acute perturbation . J Clin Invest. 1991;88:1338-1345.Crossref 16. Yeagle PL. Lipid regulation of cell membrane structure and function . FASEB J. 1989;3:1833-1842. 17. Spector AA, Yorek MA. Membrane lipid composition and cellular function . J Lipid Res. 1985;26:1015-1035. 18. Abrahamsson S, Dahlen B, Lofgren H, Pascher I, Sundell S. Molecular arrangement and confirmation of lipids of relevance to membrane structure . In: Abrahamsson S, ed. Structure of Biological Membranes . 1977:1-23. 19. Cullis PR, Hope MJ. Physical properties and functional roles of lipids in membranes . In: Vance DE, Vance JE, eds. Biochemistry of Lipids and Membranes . Menlo Park, Calif: The Benjamin Cummings Publishing Co Inc; 1985:25-72. 20. Hou SYE, Mitra AK, White SH, Menon GK, Ghadially R, Elias PM. Membrane structures in normal and essential fatty acid deficient stratum corneum: characterization by ruthenium tetroxide staining and x-ray diffraction . J Invest Dermatol. 1991;96:215-223.Crossref 21. Abraham W, Downing DT. Preparation of model membranes for skin permeability studies using stratum corneum lipids . J Invest Dermatol. 1989;93:809-813.Crossref 22. Wertz PW, Abraham W, Landmann L, Downing DT. Preparation of liposomes from stratum corneum lipids . J Invest Dermatol. 1986;87:582-584.Crossref 23. Lampe MA, Burlingame AL, Whitney J, et al. Human stratum corneum lipids: characterization and regional variations . J Lipid Res. 1983;24:120-130. 24. Menon GK, Grayson S, Brown BE, Elias PM. Lipokeratinocytes of the epidermis of a cetacean (Phocena phocena): histochemistry, ultrastructure, and lipid composition . Cell Tissue Res. 1986; 244:385-394.Crossref 25. Squier CA, Cox P, Wertz PW. Lipid content and water permeability of skin and oral mucosa . J Invest Dermatol. 1991;96: 123-126.Crossref 26. Grubauer G, Feingold KR, Elias PM. Lipid content and lipid type as determinants of the epidermal permeability barrier . J Lipid Res. 1989;30:89-96. 27. Imokawa G, Akasaki S, Hattori M, Yoshizuka N. Selective recovery of deranged water-holding properties by stratum corneum lipids . J Invest Dermatol . 1986;87:758-761.Crossref 28. Imokawa G, Akasaki S, Minematsu, Y, Kawai M. Importance of intercellular lipids in water-retention properties of the stratum corneum: induction and recovery study of surfactant dry skin . Arch Dermatol Res. 1989;281:45-51.Crossref 29. Ghadially RG, Halkier-Sorensen L, Elias PM. The effects of petrolatum on stratum corneum structure and function . J Am Acad Dermatol. 1992;26:387-396.Crossref 30. Elias PM, Williams ML. Neutral lipid storage disease with ichthyosis: defective lamellar body contents and intercellular dispersion . Arch Dermatol. 1985;121:1000-1008.Crossref 31. Koone MD, Rizzo WB, Elias PM, Williams ML, Lightner V, Pinnell SR. Ichthyosis, mental retardation, and asymptomatic spasticity: a new neurocutaneous syndrome with normal fatty alcohol: NAD+ oxidoreductase activity . Arch Dermatol. 1990;126:1485-1490.Crossref 32. Menon GK, Feingold KR, Man MQ, Schaude M, Elias PM. Structural basis for the barrier abnormality following inhibition of HMG CoA reductase in murine epidermis . J Invest Dermatol. 1992; 98:209-219.Crossref 33. Elias PM, Williams ML, Maloney ME, et al. Stratum corneum lipids in disorders of cornification: steroid sulfatase and cholesterol sulfate in normal desquamation and the pathogenesis of recessive X-linked ichthyosis . J Clin Invest. 1984;74:1414-1421.Crossref 34. Freinkel RK, Traczyk TN. Acid hydrolases of the epidermis: subcellular localization and relationship to cornification . J Invest Dermatol. 1985;80:441-446.Crossref 35. Menon GK, Grayson S, Elias PM. Cytochemical and biochemical localization of lipase and sphingomyelinase activity in mammalian epidermis . J Invest Dermatol. 1986;86:591-597.Crossref 36. Elias PM, Menon GK, Grayson S, Brown BE. Membrane structural alterations in murine stratum corneum: relationship to the localization of polar lipids and phospholipases . J Invest Dermatol. 1988;91:3-10.Crossref 37. Bergers M, Verhagen DR, Jongerius M, Van der Kerkhof PCM, Mier PD. A unique phospholipase A2 in human epidermis: its physiological functions and its level in certain dermatoses . J Invest Dermatol. 1988;90:23-25.Crossref 38. Hansen HS, Jensen B. Essential function of linoleic acid esterified in acylglycosylceramide and acylceramide in maintaining the epidermal water permeability barrier: evidence from feeding studies with linoleate, oleate, arachidonate, columbinate, and alphalinolenate . Biochim Biophys Acta . 1985;834:357-363.Crossref 39. Elliott WJ, Huo ZY, Meyer PE, Echols BS, Forats T. Dose-response and time-course of distribution of columbinic acid in rat skin . FASEB J. 1988;2:A1064.

Journal

Archives of DermatologyAmerican Medical Association

Published: Jun 1, 1993

References