Tight junction dysfunction in the stratum granulosum leads to aberrant stratum corneum barrier function in claudin-1-deficient mice

Journal of Dermatological Science

Volumn 70, Issue 1, 2013, Pages 12-18

  Sugawara, Tomoko ^a   Iwamoto, Noriko ^a   Akashi, Masaya ^a   Kojima, Taro ^b   Hisatsune, Junzo ^b   Sugai, Motoyuki ^b   Furuse, Mikio ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Claudin 1; Epidermal barrier function; Stratum corneum; Stratum granulosum; TEWL

Indexed keywords

BETA GALACTOSIDASE; CLAUDIN 1; FILAGGRIN; GLUCOSYLCERAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL JUNCTION; CELL STRUCTURE; CONTROLLED STUDY; DEHYDRATION; ENZYME ACTIVITY; EPIDERMIS; EPIDERMIS GRANULAR LAYER; EVAPORATION; HYDRATION; LIPID COMPOSITION; MOUSE; NEWBORN; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; SCANNING ELECTRON MICROSCOPY; SKIN; SKIN SURFACE; STRATUM CORNEUM; TIGHT JUNCTION; WRINKLE;

ANIMALS; ANIMALS, NEWBORN; BODY WATER; CLAUDIN-1; DEHYDRATION; EPIDERMIS; FEMALE; LIPID METABOLISM; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, SCANNING; TIGHT JUNCTIONS; WATER LOSS, INSENSIBLE;

EID: 84875808184     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2013.01.002     Document Type: Article

References (53)

1. Nemes Z., Steinert P.M. Bricks and mortar of the epidermal barrier. Exp Mol Med 1999, 31:5-19.
2. 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.
3. Hitomi K. Transglutaminases in skin epidermis. Eur J Dermatol 2005, 15:313-319.
4. Mack J.W., Steven A.C., Steinert P.M. The mechanism of interaction of filaggrin with intermediate filaments. The ionic zipper hypothesis. J Mol Biol 1993, 232:50-66.
5. Sandilands A., Sutherland C., Irvine A.D., McLean W.H. Filaggrin in the frontline: role in skin barrier function and disease. J Cell Sci 2009, 122:1285-1294.
6. Ovaere P., Lippens S., Vandenabeele P., Declercq W. The emerging roles of serine protease cascades in the epidermis. Trends Biochem Sci 2009, 34:453-463.
7. Madison K.C. Barrier function of the skin: " la raison d'etre" of the epidermis. J Invest Dermatol 2003, 121:231-241.
8. Feingold K.R. Thematic review series: skin lipids. The role of epidermal lipids in cutaneous permeability barrier homeostasis. J Lipid Res 2007, 48:2531-2546.
9. 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.
10. Uchida Y., Hara M., Nishio H., Sidransky E., Inoue S., Otsuka F., et al. Epidermal sphingomyelins are precursors for selected stratum corneum ceramides. J Lipid Res 2000, 41:2071-2082.
11. Redoules D., Tarroux R., Perie J. Epidermal enzymes: their role in homeostasis and their relationships with dermatoses. Skin Pharmacol Appl Skin Physiol 1998, 11:183-192.
12. Proksch E., Brandner J.M., Jensen J.M. The skin: an indispensable barrier. Exp Dermatol 2008, 17:1063-1072.
13. Farquhar M.G., Palade G.E. Junctional complexes in various epithelia. J Cell Biol 1963, 17:375-412.
14. Furuse M., Tsukita S. Claudins in occluding junctions of humans and flies. Trends Cell Biol 2006, 16:181-188.
15. Van Itallie C.M., Anderson J.M. Claudins and epithelial paracellular transport. Annu Rev Physiol 2006, 68:403-429.
16. Angelow S., Ahlstrom R., Yu A.S. Biology of claudins. Am J Physiol Renal Physiol 2008, 295:F867-F876.
17. Brandner J.M., Kief S., Grund C., Rendl M., Houdek P., Kuhn 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.
18. Furuse M., Hata M., Furuse K., Yoshida Y., Haratake A., Sugitani Y., 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.
19. Yuki T., Haratake A., Koishikawa H., Morita K., Miyachi Y., Inoue S. Tight junction proteins in keratinocytes: localization and contribution to barrier function. Exp Dermatol 2007, 16:324-330.
20. Kurasawa M., Kuroda S., Kida N., Murata M., Oba A., Yamamoto T., et al. Regulation of tight junction permeability by sodium caprate in human keratinocytes and reconstructed epidermis. Biochem Biophys Res Commun 2009, 381:171-175.
21. Kirschner N., Houdek P., Fromm M., Moll I., Brandner J.M. Tight junctions form a barrier in human epidermis. Eur J Cell Biol 2010, 89:839-842.
22. Hadj-Rabia S., Baala L., Vabres P., Hamel-Teillac D., Jacquemin E., Fabre M., et al. Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease. Gastroenterology 2004, 127:1386-1390.
23. Feldmeyer L., Huber M., Fellmann F., Beckmann J.S., Frenk E., Hohl D. Confirmation of the origin of NISCH syndrome. Hum Mutat 2006, 27:408-410.
24. De Benedetto A., Rafaels N.M., McGirt L.Y., Ivanov A.I., Georas S.N., Cheadle C., et al. Tight junction defects in patients with atopic dermatitis. J Allergy Clin Immunol 2011, 127:773-786. e771-7.
25. Kirschner N., Poetzl C., von den Driesch P., Wladykowski E., Moll I., Behne M.J., et al. Alteration of tight junction proteins is an early event in psoriasis: putative involvement of proinflammatory cytokines. Am J Pathol 2009, 175:1095-1106.
26. Yamaguchi T., Hayashi T., Takami H., Nakasone K., Ohnishi M., Nakayama K., et al. Phage conversion of exfoliative toxin A production in Staphylococcus aureus. Mol Microbiol 2000, 38:694-705.
27. Hardman M.J., Sisi P., Banbury D.N., Byrne C. Patterned acquisition of skin barrier function during development. Development 1998, 125:1541-1552.
28. Leyvraz C., Charles R.P., Rubera I., Guitard M., Rotman S., Breiden B., et al. The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J Cell Biol 2005, 170:487-496.
29. Sakai S., Endo Y., Ozawa N., Sugawara T., Kusaka A., Sayo T., et al. Characteristics of the epidermis and stratum corneum of hairless mice with experimentally induced diabetes mellitus. J Invest Dermatol 2003, 120:79-85.
30. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959, 37:911-917.
31. Hachem J.P., Crumrine D., Fluhr J., Brown B.E., Feingold K.R., Elias P.M. pH directly regulates epidermal permeability barrier homeostasis, and stratum corneum integrity/cohesion. J Invest Dermatol 2003, 121:345-353.
32. Yuki T., Yoshida H., Akazawa Y., Komiya A., Sugiyama Y., Inoue S. Activation of TLR2 enhances tight junction barrier in epidermal keratinocytes. J Immunol 2011, 187:3230-3237.
33. Amagai M., Matsuyoshi N., Wang Z.H., Andl C., Stanley J.R. Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1. Nat Med 2000, 6:1275-1277.
34. Nishifuji K., Shimizu A., Ishiko A., Iwasaki T., Amagai M. Removal of amino-terminal extracellular domains of desmoglein 1 by staphylococcal exfoliative toxin is sufficient to initiate epidermal blister formation. J Dermatol Sci 2010, 59:184-191.
35. Choi M.J., Maibach H.I. Role of ceramides in barrier function of healthy and diseased skin. Am J Clin Dermatol 2005, 6:215-223.
36. Holleran W.M., Takagi Y., Imokawa G., Jackson S., Lee J.M., Elias P.M. Beta-glucocerebrosidase activity in murine epidermis: characterization and localization in relation to differentiation. J Lipid Res 1992, 33:1201-1209.
37. Takagi Y., Kriehuber E., Imokawa G., Elias P.M., Holleran W.M. Beta-glucocerebrosidase activity in mammalian stratum corneum. J Lipid Res 1999, 40:861-869.
38. Brown S.J., McLean W.H. One remarkable molecule: filaggrin. J Invest Dermatol 2012, 132:751-762.
39. Smith F.J., Irvine A.D., Terron-Kwiatkowski A., Sandilands A., Campbell L.E., Zhao Y., et al. Loss-of-function mutations in the gene encoding filaggrin cause ichthyosis vulgaris. Nat Genet 2006, 38:337-342.
40. Moniaga C.S., Egawa G., Kawasaki H., Hara-Chikuma M., Honda T., Tanizaki H., et al. Flaky tail mouse denotes human atopic dermatitis in the steady state and by topical application with Dermatophagoides pteronyssinus extract. Am J Pathol 2010, 176:2385-2393.
41. 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.
42. Hashimoto K. Intercellular spaces of the human epidermis as demonstrated with lanthanum. J Invest Dermatol 1971, 57:17-31.
43. Ishida-Yamamoto A., Kishibe M., Murakami M., Honma M., Takahashi H., Iizuka H. Lamellar granule secretion starts before the establishment of tight junction barrier for paracellular tracers in mammalian epidermis. PLoS ONE 2012, 7:e31641.
44. Kubo A., Nagao K., Yokouchi M., Sasaki H., Amagai M. External antigen uptake by Langerhans cells with reorganization of epidermal tight junction barriers. J Exp Med 2009, 206:2937-2946.
45. Imokawa G., Abe A., Jin K., Higaki Y., Kawashima M., Hidano A. Decreased level of ceramides in stratum corneum of atopic dermatitis: an etiologic factor in atopic dry skin?. J Invest Dermatol 1991, 96:523-526.
46. Motta S., Monti M., Sesana S., Caputo R., Carelli S., Ghidoni R. Ceramide composition of the psoriatic scale. Biochim Biophys Acta 1993, 1182:147-151.
47. Paige D.G., Morse-Fisher N., Harper J.I. Quantification of stratum corneum ceramides and lipid envelope ceramides in the hereditary ichthyoses. Br J Dermatol 1994, 131:23-27.
48. Ishikawa J., Narita H., Kondo N., Hotta M., Takagi Y., Masukawa Y., et al. Changes in the ceramide profile of atopic dermatitis patients. J Invest Dermatol 2010, 130:2511-2514.
49. Bouwstra J.A., Gooris G.S., Dubbelaar F.E., Weerheim A.M., Ijzerman A.P., Ponec M. Role of ceramide 1 in the molecular organization of the stratum corneum lipids. J Lipid Res 1998, 39:186-196.
50. Holleran W.M., Ginns E.I., Menon G.K., Grundmann J.U., Fartasch M., McKinney C.E., et al. Consequences of beta-glucocerebrosidase deficiency in epidermis. Ultrastructure and permeability barrier alterations in Gaucher disease. J Clin Invest 1994, 93:1756-1764.
51. Holleran W.M., Takagi Y., Uchida Y. Epidermal sphingolipids: metabolism, function, and roles in skin disorders. FEBS Lett 2006, 580:5456-5466.
52. Matsui T., Kinoshita-Ida Y., Hayashi-Kisumi F., Hata M., Matsubara K., Chiba M., et al. Mouse homologue of skin-specific retroviral-like aspartic protease involved in wrinkle formation. J Biol Chem 2006, 281:27512-27525.
53. Kawasaki H., Nagao K., Kubo A., Hata T., Shimizu A., Mizuno H., et al. Altered stratum corneum barrier and enhanced percutaneous immune responses in filaggrin-null mice. J Allergy Clin Immunol 2012, 129:1538-1546.