The skin: An indispensable barrier

Experimental Dermatology

Volumn 17, Issue 12, 2008, Pages 1063-1072

  Proksch, Ehrhardt ^a   Brandner, Johanna M ^b   Jensen, Jens Michael ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Epidermal differentiation; Lipids; Skin barrier function; Stratum corneum; Tight junction

Indexed keywords

CALCIUM; CERAMIDE; CHOLESTEROL; CYCLIC AMP; CYTOKINE; FATTY ACID; FILAGGRIN; GAP JUNCTION PROTEIN; KERATIN; LIPID;

ARTICLE; ATOPIC DERMATITIS; CALCIUM TRANSPORT; CELL TRANSPORT; CYTOKINE PRODUCTION; DESMOSOME; EPIDERMIS; GAP JUNCTION; GENE MUTATION; GENETIC POLYMORPHISM; HUMAN; HYDRATION; IMMUNOPATHOLOGY; KERATINOCYTE; NONHUMAN; PERMEABILITY BARRIER; PROTEIN FUNCTION; RISK FACTOR; SIGNAL TRANSDUCTION; SKIN CELL; SKIN DISEASE; SKIN PENETRATION; SKIN PERMEABILITY; SKIN PROTECTION; SKIN STRUCTURE; SKIN WATER LOSS; STRATUM CORNEUM; TIGHT JUNCTION;

ANIMALS; CELL COMMUNICATION; EPIDERMIS; HUMANS; INTERCELLULAR JUNCTIONS; MODELS, BIOLOGICAL; PERMEABILITY; SIGNAL TRANSDUCTION; SKIN DISEASES; SKIN PHYSIOLOGICAL PHENOMENA;

EID: 56349089597     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2008.00786.x     Document Type: Article

References (107)

1. Madison K C. Barrier function of the skin: "la raison d'etre" of the epidermis. J Invest Dermatol 2003: 121: 231-242.
2. Palmer C N, Irvine A D, Terron-Kwiatkowski A et al. Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat Genet 2006: 38: 441-446.
3. Roop D. Defects in the barrier. Science 1995: 267: 474-475.
4. Nemes Z, Steinert P M. Bricks and mortar of the epidermal barrier. Exp Mol Med 1999: 31: 5-19.
5. Smith F J, Irvine A D, Terron-Kwiatkowski A et al. Loss of function mutations in the gene encoding filaggrin cause ichthyosis vulgaris. Nat Genet 2006: 38: 337-342.
6. Irvine A D, McLean W H. Breaking the (un)sound barrier: Filaggrin is a major gene for atopic dermatitis. J Invest Dermatol 2006: 126: 1200-1202.
7. Presland R B, Coulombe P A, Eckert R L, Mao-Qiang M, Feingold K R, Elias P M. Barrier function in transgenic mice overexpressing K16, involucrin, and filaggrin in the suprabasal epidermis. J Invest Dermatol 2004: 123: 603-606.
8. Presland R B, Boggess D, Lewis S P, Hull C, Fleckman P, Sundberg J P. Loss of normal profilaggrin and filaggrin in flaky tail (ft/ft) mice: An animal model for the filaggrin-deficient skin disease ichthyosis vulgaris. J Invest Dermatol 2000: 115: 1072-1081.
9. Candi E, Schmidt R, Melino G. The cornified envelope: A model of cell death in the skin. Nat Rev Mol Cell Biol 2005: 6: 328-340.
10. Matsuki M, Yamashita F, Ishida-Yamamoto A et al. Defective stratum corneum and early neonatal death in mice lacking the gene for transglutaminase 1 (keratinocyte transglutaminase). Proc Natl Acad Sci USA 1998: 95: 1044-1049.
11. Huber M, Rettler I, Bernasconi K et al. Mutations of keratinocyte transglutaminase in lamellar ichthyosis. Science 1995: 267: 525-528.
12. Egberts F, Heinrich M, Jensen J M et al. Cathepsin D is involved in the regulation of transglutaminase 1 and epidermal differentiation. J Cell Sci 2004: 117: 2295-2307.
13. Ekanayake-Mudiyanselage S, Aschauer H, Schmook F P, Jensen J M, Meingassner J G, Proksch E. Expression of epidermal keratins and the cornified envelope protein involucrin is influenced by permeability barrier disruption. J Invest Dermatol 1998: 111: 517-523.
14. Djian P, Easley K, Green H. Targeted ablation of the murine involucrin gene. J Cell Biol 2000: 151: 381-388.
15. Ishida-Yamamoto A, Iizuka H. Structural organization of cornified cell envelopes and alterations in inherited skin disorders. Exp Dermatol 1998: 7: 1-10.
16. Koch P J, de Viragh P A, Scharer E et al. Lessons from loricrin-deficient mice: Compensatory mechanisms maintaining skin barrier function in the absence of a major cornified envelope protein. J Cell Biol 2000: 151: 389-400.
17. Maestrini E, Monaco A P, McGrath J A et al. A molecular defect in loricrin, the major component of the cornified cell envelope, underlies Vohwinkel's syndrome. Nature Genet 1996: 13: 70-77.
18. Koch P J, Franke W W. Desmosomal cadherins: Another growing multigene family of adhesion molecules. Curr Opin Cell Biol 1994: 6: 682-687.
19. Al-Amoudi A, Dubochet J, Norlén L. Nanostructure of the epidermal extracellular space as observed by cryo-electron microscopy of vitreous sections of human skin. J Invest Dermatol 2005: 124: 764-777.
20. Descargues P, Deraison C, Bonnart C et al. Spink5-deficient mice mimic Netherton syndrome through degradation of desmoglein 1 by epidermal protease hyperactivity. Nat Genet 2005: 37: 56-65.
21. Swartzendruber D C, Wertz P W, Madison K C, Downing D T. Evidence that the corneocyte has a chemically bound lipid envelope. J Invest Dermatol 1987: 88: 709-713.
22. Marekov L N, Steinert P M. Ceramides are bound to structural proteins of the human foreskin epidermal cornified cell envelope. J Biol Chem 1998: 273: 17763-17770.
23. Oren A, Ganz T, Liu L, Meerloo T. In human epidermis, beta-defensin 2 is packaged in lamellar bodies. Exp Mol Pathol 2003: 74: 180-182.
24. Downing D T, Stewart M E, Wertz P W, Colton S W, Abraham W, Strauss J S. Skin lipids: An update. J Invest Dermatol 1987: 88: 2s-6s.
25. Holleran W M, Takagi Y, Menon G K, Legler G, Feingold K R, Elias P M. Processing of epidermal glucosylceramides is required for optimal mammalian cutaneous permeability barrier function. J Clin Invest 1993: 91: 1656-1664.
26. Jensen J M, Schutze S, Forl M, Kronke M, Proksch E. Roles for tumor necrosis factor receptor p55 and sphingomyelinase in repairing the cutaneous permeability barrier. J Clin Invest 1999: 104: 1761-1770.
27. Uchida Y, Hamanaka S. Stratum corneum ceramides: Function, origins, and therapeutic implications. In: Elias P M, Feingold K R, eds. Skin Barrier. New York: Taylor and Francis, 2006: 43-64.
28. Bouwstra J A, Pilgrim K, Ponec M. Structure of the skin barrier. In: Elias P M, Feingold K R, eds. Skin Barrier. New York: Taylor and Francis, 2006: 65-95.
29. Proksch E, Feingold K R, Elias P M. Epidermal HMG CoA reductase activity in essential fatty acid deficiency: Barrier requirements rather than eicosanoid generation regulate cholesterol synthesis. J Invest Dermatol 1992: 99: 216-220.
30. Herrmann T, van der Hoeven F, Grone H J et al. Mice with targeted disruption of the fatty acid transport protein 4 (Fatp 4, Slc27a4) gene show features of lethal restrictive dermopathy. J Cell Biol 2003: 161: 1105-1115.
31. Man M Q, Choi E H, Schmuth M et al. Basis for improved permeability barrier homeostasis induced by PPAR and LXR activators: Liposensors stimulate lipid synthesis, lamellar body secretion, and post-secretory lipid processing. J Invest Dermatol 2006: 126: 386-392.
32. Proksch E, Elias P M, Feingold K R. Regulation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase activity in murine epidermis. Modulation of enzyme content and activation state by barrier requirements. J Clin Invest 1990: 85: 874-882.
33. Lefevre C, Audebert S, Jobard F et al. Mutations in the transporter ABCA12 are associated with lamellar ichthyosis type 2. Hum Mol Genet 2003: 12: 2369-2378.
34. Kelsell D P, Norgett E E, Unsworth H et al. Mutations in ABCA12 underlie the severe congenital skin disease harlequin ichthyosis. Am J Hum Genet 2005: 76: 794-803.
35. Epstein E H Jr, Leventhal M E. Steroid sulfatase of human leukocytes and epidermis and the diagnosis of recessive X-linked ichthyosis. J Clin Invest 1981: 67: 1257-1262.
36. Thauvin-Robinet C, Mugneret F, Callier P et al. Unique survival in chrondrodysplasia-hermaphrodism syndrome. Am J Med Genet A 2005: 132: 335-337.
37. Sato J, Denda M, Nakanishi J, Nomura J, Koyama J. Cholesterol sulfate inhibits proteases that are involved in desquamation of stratum corneum. Invest Dermatol 1998: 111: 189-193.
38. Elias P M, Fritsch P, Epstein E H. Staphylococcal scalded skin syndrome. Clinical features, pathogenesis, and recent microbiological and biochemical developments. Arch Dermatol 1977: 113: 207-219.
39. Honari S. Topical therapies and antimicrobials in the management of burn wounds. Crit Care Nurs Clin North Am 2004: 16: 1-11.
40. Grubauer G, Elias P M, Feingold K R. Transepidermal water loss: The signal for recovery of barrier structure and function. J Lipid Res 1989: 30: 323-333.
41. Proksch E, Holleran W M, Menon G K, Elias P M, Feingold K R. Barrier function regulates epidermal lipid and DNA synthesis. Br J Dermatol 1993: 128: 473-482.
42. Proksch E, Feingold K R, Man M Q, Elias P M. Barrier function regulates epidermal DNA synthesis. J Clin Invest 1991: 87: 1668-1673.
43. Wood L C, Jackson S M, Elias P M, Grunfeld C, Feingold K R. Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice. J Clin Invest 1992: 90: 482-487.
44. Brandner J M, Kief S, Wladykowski E, Houdek P, Moll I. Tight junction proteins in the skin. Skin Pharmacol Physiol 2006: 19: 71-77.
45. Brandner J M, Proksch E. Epidermal barrier function: Role of tight junctions. In: Elias P M, Feingold K R, eds. Skin Barrier. New York: Taylor and Francis, 2006: 191-210.
46. Pummi K, Malminen M, Aho H, Karvonen S-L, Peltonen J, Peltonen S. Epidermal tight junctions: ZO-1 and occludin are expressed in mature, developing, and affected skin and in vitro differentiating keratinocytes. J Invest Dermatol 2001: 117: 1050-1058.
47. Brandner J M, Kief S, Grund C et al. Organization and formation of the tight junction system in human epidermis and cultured keratinocytes. Eur J Cell Biol 2002: 81: 253-263.
48. Langbein L, Grund C, Kuhn C et al. Tight junctions and compositionally related junctional structures in mammalian stratified epithelia and cell cultures derived therefrom. Eur J Cell Biol 2002: 81: 419-435.
49. Brandner J M, McIntyre M, Kief S, Wladykowski E, Moll I. Expression and localization of tight junction-associated proteins in human hair follicles. Arch Dermatol Res 2003: 295: 211-221.
50. Wilke K, Wepf R, Keil F J, Wittern K P, Wenck H, Biel S S. Are sweat glands an alternate penetration pathway? Understanding the morphological complexity of the axillary sweat gland apparatus. Skin Pharmacol Physiol 2006: 19: 38-49.
51. Yoshida Y, Morita K, Mizoguchi A, Ide C, Miyachi Y. Altered expression of occludin and tight junction formation in psoriasis. Arch Dermatol Res 2001: 293: 239-244.
52. Ohnemus U, Kohrmeyer K, Houdek P et al. Regulation of epidermal tight junctions (TJ) during infection with exfoliative toxin-negative Staphylococcus strains. J Invest Dermatol 2007: In press.
53. Furuse M, Hata M, Furuse K et al. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: A lesson from claudin-1-deficient mice. J Cell Biol 2002: 156: 1099-1111.
54. Hadj-Rabia S, Baala L, Vabres P et al. Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: A tight junction disease. Gastroenterology 2004: 127: 1386-1390.
55. Tunggal J A, Helfrich I, Schmitz A et al. E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J 2005: 24: 1146-1156.
56. Leyvraz C, Charles R P, Rubera I et al. The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J Cell Biol 2005: 170: 487-496.
57. Troy T C, Rahbar R, Arabzadeh A, Cheung R M, Turksen K. Delayed epidermal permeability barrier formation and hair follicle aberrations in Inv-Cldn6 mice. Mech Dev 2005: 122: 805-819.
58. Van Itallie C M, Anderson J M. Claudins and epithelial paracellular transport. Annu Rev Physiol 2006: 68: 403-429.
59. Elias P M, Matsuyoshi N, Wu H et al. Desmoglein isoform distribution affects stratum corneum structure and function. J Cell Biol 2001: 153: 243-249.
60. Trautmann A, Altznauer F, Akdis M et al. The differential fate of cadherins during T-cell-induced keratinocyte apoptosis leads to spongiosis in eczematous dermatitis. J Invest Dermatol 2001: 117: 927-934.
61. Maretzky T, Reiss K, Ludwig A et al. ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci USA 2005: 102: 9182-9187.
62. Maass K, Ghanem A, Kim J S et al. Defective epidermal barrier in neonatal mice lacking the C-terminal region of connexin43. Mol Biol Cell 2004: 15: 4597-4608.
63. Lucke T, Choudhry R, Thom R, Selmer I S, Burden A D, Hodqins M B. Upregulation of connexin 26 is a feature of keratinocyte differentiation in hyperproliferative epidermis, vaginal epithelium, and buccal epithelium. J Invest Dermatol 1999: 112: 354-361.
64. Coutinho P, Qiu C, Frank S, Tamber K, Becker D. Dynamic changes in connexin expression correlate with key events in the wound healing process. Cell Biol Int 2003: 27: 525-541.
65. Brandner J M, Houdek P, Husing B, Kaiser C, Moll I. Connexins 26, 30, and 43: Differences among spontaneous, chronic, and accelerated human wound healing. J Invest Dermatol 2004: 122: 1310-1320.
66. Richard G. Connexin disorders of the skin. Clin Dermatol 2005: 23: 23-32.
67. Meyer C G, Amedofu G K, Brandner J M, Pohland D, Timmann C, Horstmann R D. Selection for deafness? Nat Med 2002: 8: 1332-1333.
68. Man Y K, Trolove C, Tattersall D et al. A deafness-associated mutant human connexin 26 improves the epithelial barrier in vitro. J Membr Biol 2007: 218: 29-37.
69. Djalilian A R, McGaughey D, Patel S et al. Connexin 26 regulates epidermal barrier and wound remodeling and promotes psoriasiform response. J Clin Invest 2006: 116: 1243-1253.
70. Porter R M, Leitgeb S, Melton D W, Swensson O, Eady R A, Magin T M. Gene targeting at the mouse cytokeratin 10 locus: Severe skin fragility and changes of cytokeratin expression in the epidermis. J Cell Biol 1996: 132: 925-936.
71. Jensen J M, Schütze S, Neumann C, Proksch E. Impaired cutaneous permeability barrier function, skin hydration, and sphingomyelinase activity in keratin 10 deficient mice. J Invest Dermatol 2000: 115: 708-713.
72. Thune P, Nilsen T, Hanstad I K, Gustavsen T, Lövig Dahl H. The water barrier function of the skin in relation to the water content of stratum corneum, pH and skin lipids. The effect of alkaline soap and syndet on dry skin in elderly, non-atopic patients. Acta Derm Venereol 1988: 68: 277-283.
73. Proksch E, Fölster-Holst R, Jensen J M. Skin barrier function, epidermal proliferation and differentiation in eczema. J Dermatol Sci 2006: 43: 159-169.
74. Lodén M, Andersson A C, Lindberg M. Improvement in skin barrier function in patients with atopic dermatitis after treatment with a moisturizing cream (Canoderm). Br J Dermatol 1999: 140: 264-267.
75. Scott I R, Harding C R. Filaggrin breakdown to water binding compounds during development of the rat stratum corneum is controlled by the water activity of the environment. Dev Biol 1986: 115: 84-92.
76. Wang X P, Schunck M, Kallen K J et al. The interleukin-6 cytokine system regulates epidermal permeability barrier homeostasis. J Invest Dermatol 2004: 123: 124-131.
77. Lee S H, Elias P M, Proksch E, Menon G K, Mao-Quiang M, Feingold K R. Calcium and potassium are important regulators of barrier homeostasis in murine epidermis. J Clin Invest 1992: 89: 530-538.
78. Hitomi K. Transglutaminases in skin epidermis. Eur J Dermatol 2005: 15: 313-319.
79. Menon G K, Grayson S, Elias P M. Ionic calcium reservoirs in mammalian epidermis: Ultrastructural localization by ion-capture cytochemistry. J Invest Dermatol 1985: 84: 508-512.
80. Menon G K, Elias P M. Ultrastructural localization of calcium in psoriatic and normal human epidermis. Arch Dermatol 1991: 127: 57-63.
81. Lavrijsen A P, Oestmann E, Hermans J, Bodde H E, Vermeer B J, Ponec M. Barrier function parameters in various keratinization disorders: transepidermal water loss and vascular response to hexyl nicotinate. Br J Dermatol 1993: 129: 547-553.
82. 2+ pumps and their modulation by phospholamban. Biochem J 1992: 286: 591-595.
83. Foggia L, Hovnanian A. Calcium pump disorders of the skin. Am J Med Genet C Semin Med Genet 2004: 131C: 20-31.
84. Hu Z, Bonifas J M, Beech J et al. Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat Genet 2000: 24: 61-65.
85. 2+ stores. J Invest Dermatol 2003: 121: 688-694.
86. Behne M J, Barry N P, Hanson K M et al. Neonatal development of the stratum corneum pH gradient: Localization and mechanisms leading to emergence of optimal barrier function. J Invest Dermatol 2003: 120: 998-1006.
87. Denda M. New methodology to improve epidermal barrier homeostasis. In: Loden M, Maibach H I, eds. Dry Skin and Moisturizer. New York: Taylor and Francis, 2006: 155-167.
88. Jensen J M, Pfeiffer S, Witt M et al. Different Effects of Pimecrolimus and Betamethasone on the Skin Barrier in Atopic Dermatitis. J Invest Dermatol 2008: In press.
89. Kolbe L, Kligman A M, Schreiner V, Stoudemayer T. Corticosteroid-induced atrophy and barrier impairment measured by non-invasive methods in human skin. Skin Res Technol 2001: 7: 73-77.
90. Endo K, Suzuki N, Yoshida O, Sato H, Fujikura Y. The barrier component and the driving force component of transepidermal water loss and their application to skin irritant tests. Skin Res Technol 2007: 13: 425-435.
91. Elias P M, Menon G K. Structural and lipid biochemical correlates of the epidermal permeability barrier. Adv Lipid Res 1991: 24: 1-26.
92. Jakasa I, Verberk M M, Esposito M, Bos J D, Kezic S. Altered penetration of polyethylene glycols into uninvolved skin of atopic dermatitis patients. J Invest Dermatol 2007: 127: 129-134.
93. Tate M, Grove G, Joch R et al. Dye exclusion as a means to measure wetness protection of human skin. Skin Res Technol 2007: 13: 293-298.
94. Segre J A. Epidermal barrier formation and recovery in skin disorders. J Clin Invest 2006: 116: 1150-1158.
95. Berger C L, Edelson R. The life cycle of cutaneous T cell lymphoma reveals opportunities for targeted drug therapy. Curr Cancer Drug Targets 2004: 4: 609-619.
96. Leung D Y. New insights into the complex gene-environment interactions evolving into atopic dermatitis. J Allergy Clin Immunol 2006: 118: 37-45.
97. Ong P Y, Leung D Y. Immune dysregulation in atopic dermatitis. Curr Allergy Asthma Rep 2006: 6: 384-389.
98. Elias P M, Feingold K R. Does the tail wag the dog? Role of the barrier in the pathogenesis of inflammatory dermatoses and therapeutic implications. Arch Dermatol 2001: 137: 1079-1081.
99. Jensen J M, Fölster-Holst R, Baranowsky A et al. Impaired sphingomyelinase activity and epidermal differentiation in atopic dermatitis. J Invest Dermatol 2004: 122: 1423-1431.
100. Zenz R, Eferl R, Kenner L et al. Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 2005: 437: 369-375.
101. Pasparakis M, Courtois G, Hafner M et al. TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature 2002: 417: 861-866.
102. Ruether A, Stoll M, Schwarz T, Schreiber S, Fölster-Holst R. Filaggrin loss-of-function variant contributes to atopic dermatitis risk in the population of Northern Germany. Br J Dermatol 2006: 155: 1093-1094.
103. Bowcock A M, Cookson W O. The genetics of psoriasis, psoriatic arthritis and atopic dermatitis. Hum Mol Genet 2004: 13 Spec No 1: R43-R55.
104. Walley A J, Chavanas S, Moffatt M F et al. Gene polymorphism in Netherton and common atopic disease. Nat Genet 2001: 29: 175-178.
105. Fölster-Holst R, Stoll M, Koch W A, Hampe J, Christophers E, Schreiber S. Lack of association of SPINK5 polymorphisms with nonsyndromic atopic dermatitis in the population of Northern Germany. Br J Dermatol 2005: 152: 1365-1367.
106. Motta S, Monti M, Sesana S, Mellesi L, Ghidoni R, Caputo R. Abnormality of water barrier function in psoriasis. Role of ceramide fractions. Arch Dermatol 1994: 130: 452-456.
107. Fartasch M. Epidermal barrier in disorders of the skin. Microsc Res Tech 1997: 38: 361-372.