Epidermal tight junction barrier function is altered by skin inflammation, but not by filaggrin-deficient stratum corneum

Journal of Dermatological Science

Volumn 77, Issue 1, 2015, Pages 28-36

  Yokouchi, Mariko ^a,b   Kubo, Akiharu ^a   Kawasaki, Hiroshi ^a,c   Yoshida, Kazue ^a,d   Ishii, Ken ^e   Furuse, Mikio ^f   Amagai, Masayuki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b Nerima General Hospital   (Japan)

^c KITASATO INSTITUTE HOSPITAL   (Japan)

^d NATIONAL CENTER FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^e TOHO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

Atopic dermatitis; Barrier deficiency; Filaggrin; Stratum corneum; Tight junction

Indexed keywords

FILAGGRIN; MESSENGER RNA; BIOTIN; HAPTEN; INTERMEDIATE FILAMENT PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; BIOTINYLATION; CONTROLLED STUDY; CUTANEOUS PARAMETERS; DERMATITIS; EPIDERMAL TIGHT JUNCTION BARRIER; FEMALE; GENE EXPRESSION; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SKIN PENETRATION; SKIN PERMEABILITY; SKIN STRUCTURE; STRATUM CORNEUM; ANIMAL; ATOPIC DERMATITIS; C57BL MOUSE; CHEMISTRY; EPIDERMIS; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; PERMEABILITY; SKIN; TIGHT JUNCTION;

ANIMALS; BIOTIN; DERMATITIS, ATOPIC; EPIDERMIS; FEMALE; GENE EXPRESSION REGULATION; HAPTENS; INFLAMMATION; INTERMEDIATE FILAMENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; PERMEABILITY; SKIN; TIGHT JUNCTIONS;

EID: 84930414555     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2014.11.007     Document Type: Article

References (45)

1. Elias P.M. Stratum corneum defensive functions: an integrated view. J Invest Dermatol 2005, 125:183-200.
2. Kubo A., Nagao K., Amagai M. Epidermal barrier dysfunction and cutaneous sensitization in atopic diseases. J Clin Invest 2012, 122:440-447.
3. 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.
4. Yoshida K., Yokouchi M., Nagao K., Ishii K., Amagai M., Kubo A. Functional tight junction barrier localizes in the second layer of the stratum granulosum of human epidermis. J Dermatol Sci 2013, 71:89-99.
5. Kirschner N., Rosenthal R., Furuse M., Moll I., Fromm M., Brandner J.M. Contribution of tight junction proteins to ion, macromolecule, and water barrier in keratinocytes. J Invest Dermatol 2013, 133:1161-1169.
6. Bieber T. Atopic dermatitis. N Engl J Med 2008, 358:1483-1494.
7. Chavanas S., Bodemer C., Rochat A., Hamel-Teillac D., Ali M., Irvine A.D., et al. Mutations in SPINK5, encoding a serine protease inhibitor, cause Netherton syndrome. Nat Genet 2000, 25:141-142.
8. Walley A.J., Chavanas S., Moffatt M.F., Esnouf R.M., Ubhi B., Lawrence R., et al. Gene polymorphism in Netherton and common atopic disease. Nat Genet 2001, 29:175-178.
9. Oji V., Eckl K-M., Aufenvenne K., Nätebus M., Tarinski T., Ackermann K., et al. Loss of corneodesmosin leads to severe skin barrier defect, pruritus, and atopy: unraveling the peeling skin disease. Am J Hum Genet 2010, 87:274-281.
10. Brown S.J., McLean W.H.I. One remarkable molecule: filaggrin. J Invest Dermatol 2012, 132:751-762.
11. Palmer C.N.A., Irvine A.D., Terron-Kwiatkowski A., Zhao Y., Liao H., Lee S.P., 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.
12. 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. e1536.
13. De Benedetto A., Kubo A., Beck L.A. Skin barrier disruption: a requirement for allergen sensitization. J Invest Dermatol 2012, 132:949-963.
14. McGrath J.A., Uitto J. The filaggrin story: novel insights into skin-barrier function and disease. Trends Mol Med 2008, 14:20-27.
15. 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.
16. Ouchi T., Kubo A., Yokouchi M., Adachi T., Kobayashi T., Kitashima D., et al. Langerhans cell antigen capture through tight junctions confers preemptive immunity in experimental staphylococcal scalded skin syndrome. J Exp Med 2011, 208:2607-2613.
17. Kaplan D.H. In vivo function of Langerhans cells and dermal dendritic cells. Trends Immunol 2010, 31:446-451.
18. Merad M., Ginhoux F., Collin M. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 2008, 8:935-947.
19. 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.
20. Gruber R., Elias P.M., Crumrine D., Lin T-K., Brandner J.M., Hachem J-P., et al. Filaggrin genotype in ichthyosis vulgaris predicts abnormalities in epidermal structure and function. Am J Pathol 2011, 178:2252-2263.
21. Tomimori Y., Tanaka Y., Goto M., Fukuda Y. Repeated topical challenge with chemical antigen elicits sustained dermatitis in NC/Nga mice in specific-pathogen-free condition. J Invest Dermatol 2005, 124:119-124.
22. Matsuda H., Watanabe N., Geba G.P., Sperl J., Tsudzuki M., Hiroi J., et al. Development of atopic dermatitis-like skin lesion with IgE hyperproduction in NC/Nga mice. Int Immunol 1997, 9:461-466.
23. Masuda S., Oda Y., Sasaki H., Ikenouchi J., Higashi T., Akashi M., et al. LSR defines cell corners for tricellular tight junction formation in epithelial cells. J Cell Sci 2011, 124:548-555.
24. Itoh M., Yonemura S., Nagafuchi A., Tsukita S. A 220-kD undercoat-constitutive protein: its specific localization at cadherin-based cell-cell adhesion sites. J Cell Biol 1991, 115:1449-1462.
25. Saitou M., Ando-Akatsuka Y., Itoh M., Furuse M., Inazawa J., Fujimoto K., et al. Mammalian occludin in epithelial cells: its expression and subcellular distribution. Eur J Cell Biol 1997, 73:222-231.
26. Kitano Y., Okada N. Separation of the epidermal sheet by dispase. Br J Dermatol 1983, 108:555-560.
27. Kubo A., Nagao K., Amagai M. 3D visualization of epidermal Langerhans cells. Methods Mol Biol 2013, 961:119-127.
28. Chen Y., Merzdorf C., Paul D.L., Goodenough D.A. COOH terminus of occludin is required for tight junction barrier function in early Xenopus embryos. J Cell Biol 1997, 138:891-899.
29. Hanakawa Y., Schechter N.M., Lin C., Garza L., Li H., Yamaguchi T., et al. Molecular mechanisms of blister formation in bullous impetigo and staphylococcal scalded skin syndrome. J Clin Invest 2002, 110:53-60.
30. Ishii K., Lin C., Siegel D.L., Stanley J.R. Isolation of pathogenic monoclonal anti-desmoglein 1 human antibodies by phage display of pemphigus foliaceus autoantibodies. J Invest Dermatol 2008, 128:939-948.
31. Higashi T., Tokuda S., Kitajiri S.-i., Masuda S., Nakamura H., Oda Y., et al. Analysis of the 'angulin' proteins LSR, ILDR1 and ILDR2-tricellulin recruitment, epithelial barrier function and implication in deafness pathogenesis. J Cell Sci 2013, 126:966-977.
32. Ikenouchi J., Furuse M., Furuse K., Sasaki H., Tsukita S., Tsukita S. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol 2005, 171:939-945.
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. Tsukita S., Yamazaki Y., Katsuno T., Tamura A. Tight junction-based epithelial microenvironment and cell proliferation. Oncogene 2008, 27:6930-6938.
35. Mineta K., Yamamoto Y., Yamazaki Y., Tanaka H., Tada Y., Saito K., et al. Predicted expansion of the claudin multigene family. FEBS Lett 2011, 585:606-612.
36. 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.
37. Kirschner N., Brandner J.M. Barriers and more: functions of tight junction proteins in the skin. Ann NY Acad Sci 2012, 1257:158-166.
38. Sugawara T., Iwamoto N., Akashi M., Kojima T., Hisatsune J., Sugai M., et al. Tight junction dysfunction in the stratum granulosum leads to aberrant stratum corneum barrier function in claudin-1-deficient mice. J Dermatol Sci 2013, 70:12-18.
39. Turksen K., Troy T-C. Permeability barrier dysfunction in transgenic mice overexpressing claudin 6. Development 2002, 129:1775-1784.
40. Nakai K., Yoneda K., Hosokawa Y., Moriue T., Presland R.B., Fallon P.G., et al. Reduced expression of epidermal growth factor receptor, E-cadherin, and occludin in the skin of flaky tail mice is due to filaggrin and loricrin deficiencies. Am J Pathol 2012, 181:969-977.
41. Fallon P.G., Sasaki T., Sandilands A., Campbell L.E., Saunders S.P., Mangan N.E., et al. A homozygous frameshift mutation in the mouse Flg gene facilitates enhanced percutaneous allergen priming. Nat Genet 2009, 41:602-608.
42. Sasaki T., Shiohama A., Kubo A., Kawasaki H., Ishida-Yamamoto A., Yamada T., et al. A homozygous nonsense mutation in the gene for Tmem79, a component for the lamellar granule secretory system, produces spontaneous eczema in an experimental model of atopic dermatitis. J Allergy Clin Immunol 2013, 132:1111-1120. e1114.
43. Yuki T., Hachiya A., Kusaka A., Sriwiriyanont P., Visscher M.O., Morita K., et al. Characterization of tight junctions and their disruption by UVB in human epidermis and cultured keratinocytes. J Invest Dermatol 2011, 131:744-752.
44. Yuki T., Komiya A., Kusaka A., Kuze T., Sugiyama Y., Inoue S. Impaired tight junctions obstruct stratum corneum formation by altering polar lipid and profilaggrin processing. J Dermatol Sci 2013, 69:148-158.
45. Anderson J.M. Molecular structure of tight junctions and their role in epithelial transport. News Physiol Sci 2001, 16:126-130.