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Glycerol Regulates Stratum Corneum Hydration in Sebaceous Gland Deficient (Asebia) Mice

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Glycerol Regulates Stratum Corneum Hydration in Sebaceous Gland Deficient (Asebia) Mice CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector ORIGINAL ARTICLE See related Commentary on page iv Glycerol Regulates Stratum Corneum Hydration in Sebaceous Gland De¢cient (Asebia) Mice Joachim W. Fluhr,nz1 Man Mao-Qiang,n1 Barbara E. Brown,n Philip W.Wertz,w Debra Crumrine,n John P. Sundberg,y Kenneth R. Feingold,nz and Peter M. Eliasn nDermatology and zMedical (Metabolism) Services,Veterans Administration Medical Center, and Departments of nDermatology and zMedicine, University of California, San Francisco, California, USA; wDows Institute, University of Iowa College of Dentistry, Iowa City, Iowa, USA; yThe Jackson Laboratory, Bar Harbor, Maine, USA; zDepartment of Dermatology, Friedrich-Schiller University, Jena, Germany The only known function of human sebaceous glands glands, normalized stratum corneum hydration, and is the provocation of acne. We assessed here whether the glycerol content of asebia stratum corneum was sebum in£uences stratum corneum hydration or per- 85% lower than in normal stratum corneum. In con- meability barrier function in asebia J1 and 2 J mice, trast, another potent endogenous humectant (urea) did with profound sebaceous gland hypoplasia. Asebia J1 not correct the abnormality.The importance of glycerol mice showed normal permeability barrier homeostasis generation from triglyceride in sebaceous glands for and extracellular lamellar membrane structures, but stratum corneum hydration was demonstrated further they displayed epidermal hyperplasia, in£ammation, by (i) the absence of sebaceous-gland-associated lipase and decreased (450%) stratum corneum hydration, activity in asebia mice, whereas abundant enzyme ac- associated with a reduction in sebaceous gland lipids tivity was present in the glands of control mice; and (wax diesters/monoesters, sterol esters). The triglyceride (ii) the inability of high concentrations of topical trigly- content of both asebia and control stratum corneum ceride to correct the hydration abnormality, despite the was low, consistent with high rates of triglyceride hy- presence of abundant lipase activity in asebia stratum drolysis within the normal pilosebaceous apparatus, corneum. These results show that sebaceous-gland-de- despite high rates of triglyceride synthesis. Although a rived glycerol is a major contributor to stratum cor- mixture of synthetic, sebum-like lipids (sterol/wax neum hydration. Key words: asebia mice/barrier function/ esters, triglycerides) did not restore normal stratum glycerol/hydration/lipase/SCD1/sebum/triglycerides. J Invest corneum hydration to asebia skin, topical glycerol, the Dermatol 120:728 ^737, 2003 putative product of triglyceride hydrolysis in sebaceous utaneous sebaceous glands deliver sebum to the skin skin, such as that in prepubertal children, exhibits normal basal surface through a process of continuous, holocrine barrier function, it has been assumed that sebum does not secretion. Sebum comprises a complex lipid mix- in£uence epidermal permeability barrier function (Kligman, ture that is enriched in wax monoesters and diesters, 1963). But the barrier recovery kinetics of sebaceous-gland-poor with substantial species-speci¢c di¡erences in trigly- versus -enriched skin after acute insults has not been examined, Ccerides (TGs), sterol esters, free fatty acids (FFAs), and squalene and this form of stress test is a more sensitive indicator of perme- (Thody and Shuster, 1989; Stewart and Downing, 1991). Although ability barrier status than are basal assessments (Feingold and a variety of functions have been proposed for cutaneous sebac- Elias, 1999). Moreover, products of Meibomian glands (modi¢ed eous-gland-derived lipids (Nicolaides, 1974; Thody and Shuster, sebaceous glands) in£uence barrier function in conjunctival 1989), the predominant view holds that the principal role of epithelia (Bron and Ti¡any, 1998). Furthermore, after sebum is sebum in humans is negative, i.e., its well-accepted pathophysio- deposited on the surface of the SC, it inspissates into the inter- logic role in the provocation of acne (Kligman, 1963; Stewart stices (Kligman and Shelley, 1958) and interacts with the extra- and Downing, 1991). Because sebaceous-gland-impoverished cellular lamellar bilayer system (Sheu et al, 1999). There, its constituent fatty acids, which lack essential fatty acids, could di- lute or replace the linoleic acid in SC acylceramides, as proposed Manuscript received September 14, 2002; revised November 19, 2002; for follicular epithelia (Stewart et al, 1986). As a net result of one accepted for publication December 17, 2002 or more of these processes, sebum could in£uence permeability 1Each contributed equally, and therefore they should be considered co- barrier homeostasis. ¢rst authors. To assess two potential functions of cutaneous sebaceous Reprint requests to: Peter M. Elias, M.D., Dermatology Service (190), glands, we compared permeability barrier homeostasis and SC Veterans A¡airs Medical Center, 4150 Clement Street, San Francisco, CA hydration in two closely related models where sebaceous glands 94121; Email: [email protected] Abbreviations: abJ/abJ, asebia J; ab2J/ab2J, asebia 2 J; AQP3, aquaporin 3; are largely absent, the asebia mouse. Asebia mice display not only FFA, free fatty acid; PPARa, peroxisomal proliferator activator a; ScdabJ/ profound sebaceous gland hypoplasia, but also other cutaneous ScdabJ, asebia; SCD1, stearyl CoA desaturase 1 (protein); SCD1, stearyl CoA abnormalities, including mild scaling, patchy scarring alopecia, desaturase 1 (gene); TEWL, transepidermal water loss; TG, triglyceride. and epidermal hyperplasia (Gates and Karasek, 1965; Josefowicz 0022-202X/03/$15.00 . Copyright r 2003 by The Society for Investigative Dermatology, Inc. 728 VOL. 120, NO. 5 MAY 2003 ABNORMAL STRATUM CORNEUM HYDRATION IN ASEBIA MICE 729 and Hardy, 1978; Sundberg and King, 1996). Although recent aqueous toluidine blue for light microscopy and to visualize mast cell studies have shown that mutations in the gene that encodes stear- metachromasia. yl CoA desaturase 1 (SCD1) are responsible for both the asebia J1 and asebia 2 J phenotypes (Zheng et al, 1999; Sundberg et al, Lipid content analysis Full-thickness mouse skin was excised from 2000), the basis for sebaceous gland hypoplasia in these models is shaved asebia J1 and control animals, and incubated with 10 mM ethylenediamine tetraacetic acid (EDTA), pH 7.4, at 371C for 30 min to not known. We report here that, despite the presence of epider- separate epidermis from dermis (Grubauer et al, 1989). Nucleated mal hyperplasia, asebia J1 mice display normal permeability bar- epidermal cells were separated from SC by further incubation with 0.5% rier homeostasis but a profound abnormality in SC hydration. trypsin in phosphate-bu¡ered saline for 2 h, followed by vortexing. SC The hydration abnormality in asebia skin could be attributed sheets were freeze-dried, weighed, and total lipids were extracted (Bligh further to decreased glycerol generation due to a lack of endogen- and Dyer, 1959), dried, weighed, and stored at ^701C until analyzed. ous, sebaceous-gland-derived TG and associated lipase activity. Neutral lipids were separated from polar lipids by high performance The hydration abnormality in asebia mice could explain the in- thin layer chromatography, using a CAMAG linomat IV Autospotter creased propensity of sebum-depleted skin sites of humans to de- (CAMAG Scienti¢c, Washington, NC), extracted, and solubilized in velop eczematous skin disorders, particularly when subjected to chloroform:methanol (2:1 vol). Nonpolar lipids were then fractionated and quantitated (Law et al, 1995). Brie£y, 10 Â10 cm glass-backed TLC plates, xeric stress. coated with 0.25 mm thick silica gel G (Adsorbosil-plus-1; Alltech Associates, Deer¢eld, IL), were washed with chloroform:methanol (2:1) and activated in a 1101C oven; the adsorbent was scored into 6 mm wide METHODS lanes. Calibrated glass capillary tubes were used to apply 5 ml samples and chromatograms were developed in n-hexane:benzene (1:1 vol) to Animals and experimental procedures Male asebia J1 mice (ABJ/Le- 95 cm. Finally, chromatograms were developed to 5 cm with hexane:ethyl ScdabJ/ScdabJ) (The Jackson Laboratory, Bar Harbor, ME) and their normal ether:acetic acid (70:30:1), charred, and quantitated by photodensitometry. heterozygote ( þ /abJ) and wild-type ( þ / þ or þ /?) littermates, between Lipid standards were obtained from Sigma (St. Louis, MO). 6 and 10 wk of age, were utilized for most studies. Asebia 2 J (ab2J/ab2J, (The Jackson Laboratory) mice were utilized in some experiments, where Glycerol content analysis Asebia J1 and 2 J mice as well as wild-type indicated. All mice were maintained in the Animal Care Facility of the littermates were carefully shaved 24 h before collecting total SC by pooling Veterans A¡airs Medical Center, San Francisco, in a temperature- and sequential tape strips down to the glistening layer in all groups (D-Squame humidity-controlled room, and fed standard laboratory chow (Teklad 22/5 disks, CuDerm Corporation, Dallas, TX). Because of di¡erences in SC Rodent Diet) and acidi¢ed tap water ad libitum. All functional studies were thickness and cohesion ( ¼ protein per stripping) between the two groups, performed in the Animal Care Facility, and mice were anesthetized with data re£ect total glycerol/total SC protein from equivalent surface areas. chloral hydrate and/or iso£orane. SC hydration was quantitated as changes The disks
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