Perturbation of lamellar granule secretion by sodium caprate implicates epidermal tight junctions in lamellar granule function

Journal of Dermatological Science

Volumn 59, Issue 2, 2010, Pages 107-114

  Kuroda, Shohei ^a   Kurasawa, Masumi ^a   Mizukoshi, Koji ^a   Maeda, Tetsuo ^a   Yamamoto, Takuya ^a   Oba, Ai ^a   Kishibe, Mari ^b   Ishida Yamamoto, Akemi ^b  

^a POLA CHEMICAL INDUSTRIES INC   (Japan)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

Author keywords

BODIPY FL; Keratinocyte; Lamellar granule; LEKTI; Tight junction

Indexed keywords

CERAMIDE; DECANOATE SODIUM; FATTY ACID; FLUORESCENT CERAMIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL GRANULE; CELL SECRETION; CONTROLLED STUDY; ELECTRON MICROSCOPY; EPIDERMIS; EPIDERMIS CELL; HUMAN; HUMAN CELL; KERATINOCYTE; LAMELLAR BODY; MEMBRANE DEPOLARIZATION; NORMAL HUMAN; PRIORITY JOURNAL; TIGHT JUNCTION;

CELLS, CULTURED; CERAMIDES; CYTOPLASMIC GRANULES; DECANOIC ACIDS; EPIDERMIS; HUMANS; KERATINOCYTES; PROTEINASE INHIBITORY PROTEINS, SECRETORY; TIGHT JUNCTIONS;

EID: 77955039293     PISSN: 09231811     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2010.06.001     Document Type: Article

References (43)

1. Elias P.M., Cullander C., Mauro T., Rassner U., Komuves L., Brown B.E., et al. The secretory granular cell: the outermost granular cell as a specialized secretory cell. J Investig Dermatol Symp Proc 1998, 3:87-100.
2. Madison K.C., Sando G.N., Howard E.J., True C.A., Gilbert D., Swartzendruber D.C., et al. Lamellar granule biogenesis: a role for ceramide glucosyltransferase, lysosomal enzyme transport, and the Golgi. J Investig Dermatol Symp Proc 1998, 3:80-86.
3. Ishida-Yamamoto A., Simon M., Kishibe M., Miyauchi Y., Takahashi H., Yoshida S., et al. Epidermal lamellar granules transport different cargoes as distinct aggregates. J Invest Dermatol 2004, 122:1137-1144.
4. Elias P.M., Choi E.H. Interactions among stratum corneum defensive functions. Exp Dermatol 2005, 14:719-726.
5. Hayward A.F. Membrane-coating granules. Int Rev Cytol 1979, 59:97-127.
6. Odland G.F., Holbrook K. The lamellar granules of epidermis. Curr Probl Dermatol 1981, 9:29-49.
7. Milner M.E., O'Guin W.M., Holbrook K.A., Dale B.A. Abnormal lamellar granules in harlequin ichthyosis. J Invest Dermatol 1992, 99:824-829.
8. Akiyama M., Shimizu H. An update on molecular aspects of the non-syndromic ichthyosis. Exp Dermatol 2008, 17:373-382.
9. Lefevre C., Audebert S., Jobard F., Bouadjar B., Lakhdar H., Boughdene-Stambouli O., et al. Mutations in the transporter ABCA12 are associated with lamellar ichthyosis type 2. Hum Mol Genet 2003, 12:2369-2378.
10. Tartaglia-Polcini A., Bonnart C., Micheloni A., Cianfarani F., Andre A., Zambruno G., et al. SPINK5, the defective gene in Netherton syndrome, encodes multiple LEKTI isoforms derived from alternative pre-mRNA processing. J Invest Dermatol 2006, 126:315-324.
11. Hansson L., Backman A., Ny A., Edlund M., Ekholm E., Ekstrand H.B., et al. Epidermal overexpression of stratum corneum chymotryptic enzyme in mice: a model for chronic itchy dermatitis. J Invest Dermatol 2002, 118:444-449.
12. Egberts F., Heinrich F., Jensen J.M., Winoto-Morbach S., Pfeiffer S., Wickel M., et al. Cathepsin D is involved in the regulation of transglutaminase 1 and epidermal differentiation. J Cell Sci 2004, 117:2295-2307.
13. Rassner U., Feingold K.R., Crumrine D.A., Elias P.M. Coordinate assembly of lipids and enzyme proteins into epidermal lamellar bodies. Tissue Cell 1999, 31:489-498.
14. Ishida-Yamamoto A., Deraison C., Bonnart C., Bitoun E., Robinson R., O'Brien T.J., et al. LEKTI is localized in lamellar granules, separated from KLK5 and KLK7, and is secreted in the extracellular spaces of the superficial stratum granulosum. J Invest Dermatol 2005, 124:360-366.
15. Sprecher E., Ishida-Yamamoto A., Mizrahi-Koren M., Rapaport D., Goldsher D., Indelman M., et al. A mutation in SNAP29, coding for a SNARE protein involved in intracellular trafficking, causes a novel neurocutaneous syndrome characterized by cerebral dysgenesis, neuropathy, ichthyosis, and palmoplantar keratoderma. Am J Hum Genet 2005, 77:242-251.
16. Yamamoto T., Kurasawa M., Hattori T., Maeda T., Nakano H., Sasaki H. Relationship between expression of tight junction-related molecules and perturbed epidermal barrier function in UVB-irradiated hairless mice. Arch Dermatol Res 2008, 300:61-68.
17. 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.
18. 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.
19. 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.
20. Yamamoto T., Saeki Y., Kurasawa M., Kuroda S., Arase S., Sasaki H. Effect of RNA interference of tight junction-related molecules on intercellular barrier function in cultured human keratinocytes. Arch Dermatol Res 2008, 300:517-524.
21. Fartasch M., Ponec M. Improved barrier structure formation in air-exposed human keratinocyte culture systems. J Invest Dermatol 1994, 102:366-374.
22. Madison K.C., Howard E.J. Ceramides are transported through the Golgi apparatus in human keratinocytes in vitro. J Invest Dermatol 1996, 106:1030-1035.
23. Marks D.L., Singh R.D., Choudhury A., Wheatley C.L., Pagano R.E. Use of fluorescent sphingolipid analogs to study lipid transport along the endocytic pathway. Methods 2005, 36:186-195.
24. Pagano R.E., Chen C.S. Use of BODIPY-labeled sphingolipids to study membrane traffic along the endocytic pathway. Ann N Y Acad Sci 1998, 845:152-160.
25. Pagano R.E., Martin O.C., Kang H.C., Haugland R.P. A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor. J Cell Biol 1991, 13:1267-1279.
26. Chen C.S., Bach G., Pagano R.E. Abnormal transport along the lysosomal pathway in mucolipidosis, type IV disease. Proc Natl Acad Sci USA 1998, 95:6373-6378.
27. Bitoun E., Micheloni A., Lamant L., Bonnart C., Tartaglia-Polcini A., Cobbold C., et al. LEKTI proteolytic processing in human primary keratinocytes, tissue distribution and defective expression in Netherton syndrome. Hum Mol Genet 2003, 12:2417-2430.
28. Raghunath M., Tontsidou L., Oji V., Aufenvenne K., Schürmeyer-Horst F., Jayakumar A., et al. SPINK5 and Netherton syndrome: novel mutations, demonstration of missing LEKTI, and differential expression of transglutaminases. J Invest Dermatol 2004, 123:474-483.
29. Ishida-Yamamoto A., Mizukoshi K. Electron microscopic and immunoelectron microscopic examinations of the skin. J Med Technol 2006, 50:893-896.
30. Salama N.N., Eddington N.D., Fasano A. Tight junction modulation and its relationship to drug delivery. Adv Drug Deliv Rev 2006, 58:15-28.
31. Jayakumar A., Kang Y., Henderson Y., Mitsudo K., Liu X., Briggs K., et al. Consequences of C-terminal domains and N-terminal signal peptide deletions on LEKTI secretion, stability, and subcellular distribution. Arch Biochem Biophys 2005, 435:89-102.
32. Deraison C., Bonnart C., Lopez F., Besson C., Robinson R., Jayakumar A., et al. LEKTI fragments specifically inhibit KLK5, KLK7, and KLK14 and control desquamation through a pH-dependent interaction. Mol Biol Cell 2007, 18:3607-3619.
33. Matoltsy A.G., Parakkal P.F. Membrane-coating granules of keratinizing epithelia. J Cell Biol 1994, 24:297-307.
34. Merril A.H. De novo sphingolipid biosynthesis: a necessary, but dangerous, pathway. J Biol Chem 2002, 277:25843-25846.
35. Van Meer G., Lisman Q. Sphingolipid transport: rafts and translocators. J Biol Chem 2002, 277:25855-25858.
36. Watanabe R., Wu K., Paul P., Marks D.L., Kobayashi T., Pittelkow M.R., et al. Up-regulation of glycosylceramide synthase expression and activity during human keratinocyte differentiation. J Biol Chem 1998, 273:9651-9655.
37. Balda M.S., Whitney J.A., Flores C., González S., Cereijido M., Matter K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol 1996, 134(4):1031-1049.
38. Hernandez S., Chavez Munguia B., Gonzalez-Mariscal L. ZO-2 silencing in epithelial cells perturbs the gate and fence function of tight junctions and leads to an atypical monolayer architecture. Exp Cell Res 2007, 313(8):1533-1547.
39. Umeda K., Ikenouchi J., Katahira-Tayama S., Furuse K., Sasaki H., Nakayama M., et al. ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 2006, 126:741-754.
40. Yu W., Fang X., Ewald A., Wong K., Hunt C.A., Werb Z., et al. Formation of cysts by alveolar type II cells in three-dimensional culture reveals a novel mechanism for epithelial morphogenesis. Mol Biol Cell 2007, 18:1693-1700.
41. Guo Y., Martinez-Williams C., Yellowley C.E., Donahue H.J., Rannels D.E. Connexin expression by alveolar epithelial cells is regulated by extracellular matrix. Am J Physiol Lung Cell Mol Physiol 2001, 280:L191-202.
42. Roelandt T., Giddelo C., Heughebaert C., Denecker G., Hupe M., Crumrine D., et al. The " Caveolae Brake hypothesis" and the epidermal barrier. J Invest Dermatol 2009, 129:927-936.
43. Hayashi M., Tomita M. Mechanistic analysis for drug permeation through intestinal membrane. Drug Metab Pharmacokinet 2007, 22:67-77.