Monounsaturated fatty acids reduce the barrier of stratum corneum lipid membranes by enhancing the formation of a hexagonal lateral packing

Langmuir

Volumn 30, Issue 22, 2014, Pages 6534-6543

  Mojumdar, Enamul H ^a   Helder, Richard W J ^a   Gooris, Gert S ^a   Bouwstra, Joke A ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DERMATOLOGY; FATTY ACIDS;

IN-VITRO MODELS; LAMELLAR PHASIS; LIPID COMPOSITION; OUTER LAYER; PACKING DENSITY; SKIN DISEASE; STRATUM CORNEUM; STRATUM CORNEUM LIPIDS;

MONOUNSATURATED FATTY ACIDS;

ARTIFICIAL MEMBRANE; MONOUNSATURATED FATTY ACID;

ANIMAL; ARTIFICIAL MEMBRANE; CHEMISTRY; HUMAN; SKIN;

ANIMALS; FATTY ACIDS, MONOUNSATURATED; HUMANS; MEMBRANES, ARTIFICIAL; SKIN;

EID: 84902137300     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la500972w     Document Type: Article

References (60)

1. Proksch, E.; Brandner, J. M.; Jensen, J.-M. The skin: An indispensable barrier Exp. Dermatol. 2008, 17, 1063-1072
2. 2 transport through human skin in vitro Int. J. Pharm. 1989, 53, 13-24
3. Talreja, P.; Kasting, G.; Kleene, N.; Pickens, W.; Wang, T.-F. Visualization of the lipid barrier and measurement of lipid pathlength in human stratum corneum AAPS PharmSci. 2001, 3, 48-56
4. Wertz, P. W.; Miethke, M. C.; Long, S. A.; Strauss, J. S.; Downing, D. T. The composition of the ceramides from human stratum corneum and from comedones J. Investig. Dermatol. 1985, 84, 410-412
5. Robson, K. J.; Stewart, M. E.; Michelsen, S.; Lazo, N. D.; Downing, D. T. 6-Hydroxy-4-sphingenine in human epidermal ceramides J. Lipid Res. 1994, 35, 2060-2068
6. Stewart, M. E.; Downing, D. T. A new 6-hydroxy-4-sphingenine-containing ceramide in human skin J. Lipid Res. 1999, 40, 1434-1439
7. Masukawa, Y.; Narita, H.; Shimizu, E.; Kondo, N.; Sugai, Y.; Oba, T.; Homma, R.; Ishikawa, J.; Takagi, Y.; Kitahara, T.; Takema, Y.; Kita, K. Characterization of overall ceramide species in human stratum corneum J. Lipid Res. 2008, 49, 1466-1476
8. Weerheim, A.; Ponec, M. Determination of stratum corneum lipid profile by tape stripping in combination with high-performance thin-layer chromatography Arch. Dermatol. Res. 2001, 293, 191-199
9. Ponec, M.; Weerheim, A.; Lankhorst, P.; Wertz, P. New acylceramide in native and reconstructed epidermis J. Investig. Dermatol. 2003, 120, 581-588
10. Bouwstra, J. A.; Gooris, G. S.; van der Spek, J. A.; Bras, W. Structural investigations of human stratum corneum by small-angle X-ray scattering J. Investig. Dermatol. 1991, 97, 1005-1012
11. Madison, K. C.; Swartzendruber, D. C.; Wertz, P. W.; Downing, D. T. Presence of intact intercellular lipid lamellae in the upper layers of the stratum corneum J. Investig. Dermatol. 1987, 88, 714-718
12. White, S. H.; Mirejovsky, D.; King, G. I. Structure of lamellar lipid domains and corneocyte envelopes of murine stratum corneum. An X-ray diffraction study Biochemistry 1988, 27, 3725-3732
13. Hatta, I.; Ohta, N.; Inoue, K.; Yagi, N. Coexistence of two domains in intercellular lipid matrix of stratum corneum Biochim. Biophys. Acta, Biomembr. 2006, 1758, 1830-1836
14. Bommannan, D.; Potts, R. O.; Guy, R. H. Examination of stratum corneum barrier function in vivo by infrared spectroscopy J. Investig. Dermatol. 1990, 95, 403-408
15. Boncheva, M.; Damien, F.; Normand, V. Molecular organization of the lipid matrix in intact stratum corneum using ATR-FTIR spectroscopy Biochim. Biophys. Acta, Biomembr. 2008, 1778, 1344-1355
16. Ongpipattanakul, B.; Francoeur, M. L.; Potts, R. O. Polymorphism in stratum corneum lipids Biochim. Biophys. Acta, Biomembr. 1994, 1190, 115-122
17. Janssens, M.; van Smeden, J.; Gooris, G. S.; Bras, W.; Portale, G.; Caspers, P. J.; Vreeken, R. J.; Hankemeier, T.; Kezic, S.; Wolterbeek, R.; Lavrijsen, A. P.; Bouwstra, J. A. Increase in short-chain ceramides correlates with an altered lipid organization and decreased barrier function in atopic eczema patients J. Lipid Res. 2012, 53, 2755-2766
18. Potts, R. O.; Francoeur, M. L. Lipid biophysics of water loss through the skin Proc. Natl. Acad. Sci. U. S. A. 1990, 87, 3871-3873
19. Damien, F.; Boncheva, M. The extent of orthorhombic lipid phases in the stratum corneum determines the barrier efficiency of human skin in vivo J. Investig. Dermatol. 2010, 130, 611-614
20. Groen, D.; Poole, D. S.; Gooris, G. S.; Bouwstra, J. A. Is an orthorhombic lateral packing and a proper lamellar organization important for the skin barrier function? Biochim. Biophys. Acta, Biomembr. 2011, 1808, 1529-1537
21. van Smeden, J.; Hoppel, L.; van der Heijden, R.; Hankemeier, T.; Vreeken, R. J.; Bouwstra, J. A. LC/MS analysis of stratum corneum lipids: Ceramide profiling and discovery J. Lipid Res. 2011, 52, 1211-1221
22. Mojumdar, E. H.; Groen, D.; Gooris, G. S.; Barlow, D. J.; Lawrence, M. J.; Deme, B.; Bouwstra, J. A. Localization of cholesterol and fatty acid in a model lipid membrane: A neutron diffraction approach Biophys. J. 2013, 105, 911-918
23. Bonnart, C.; Deraison, C.; Lacroix, M.; Uchida, Y.; Besson, C.; Robin, A.; Briot, A.; Gonthier, M.; Lamant, L.; Dubus, P.; Monsarrat, B.; Hovnanian, A. Elastase 2 is expressed in human and mouse epidermis and impairs skin barrier function in Netherton syndrome through filaggrin and lipid misprocessing J. Clin. Investig. 2010, 120, 871-882
24. 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
25. 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
26. Ishikawa, J.; Narita, H.; Kondo, N.; Hotta, M.; Takagi, Y.; Masukawa, Y.; Kitahara, T.; Takema, Y.; Koyano, S.; Yamazaki, S.; Hatamochi, A. Changes in the ceramide profile of atopic dermatitis patients J. Invest. Dermatol. 2010, 130, 2511-2514
27. Sassa, T.; Ohno, Y.; Suzuki, S.; Nomura, T.; Nishioka, C.; Kashiwagi, T.; Hirayama, T.; Akiyama, M.; Taguchi, R.; Shimizu, H.; Itohara, S.; Kihara, A. Impaired epidermal permeability barrier in mice lacking Elovl1, the gene responsible for very-long-chain fatty acid production Mol. Cell. Biol. 2013, 33, 2787-2796
28. Park, Y.-H.; Jang, W.-H.; Seo, J. A.; Park, M.; Lee, T. R.; Park, Y.-H.; Kim, D. K.; Lim, K.-M. Decrease of ceramides with very long-chain fatty acids and downregulation of elongases in a murine atopic dermatitis model J. Invest. Dermatol. 2012, 132, 476-479
29. Pilgram, G. S. K.; Vissers, D. C. J.; van der Meulen, H.; Pavel, S.; Lavrijsen, S. P. M.; Bouwstra, J. A.; Koerten, H. K. Aberrant lipid organization in stratum corneum of patients with atopic dermatitis and lamellar ichthyosis J. Invest. Dermatol. 2001, 117, 710-717
30. Jennemann, R.; Rabionet, M.; Gorgas, K.; Epstein, S.; Dalpke, A.; Rothermel, U.; Bayerle, A.; van der Hoeven, F.; Imgrund, S.; Kirsch, J.; Nickel, W.; Willecke, K.; Riezman, H.; Gröne, H.-J.; Sandhoff, R. Loss of ceramide synthase 3 causes lethal skin barrier disruption Hum. Mol. Genet. 2012, 21, 586-608
31. Vasireddy, V.; Uchida, Y.; Salem, N.; Kim, S. Y.; Mandal, M. N. A.; Reddy, G. B.; Bodepudi, R.; Alderson, N. L.; Brown, J. C.; Hama, H.; Dlugosz, A.; Elias, P. M.; Holleran, W. M.; Ayyagari, R. Loss of functional ELOVL4 depletes very long-chain fatty acids (≥C28) and the unique ω- O -acylceramides in skin leading to neonatal death Hum. Mol. Genet. 2007, 16, 471-482
32. 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. Investig. Dermatol. 1991, 96, 523-526
33. Velkova, V.; Lafleur, M. Influence of the lipid composition on the organization of skin lipid model mixtures: An infrared spectroscopy investigation Chem. Phys. Lipids 2002, 117, 63-74
34. van Smeden, J.; Janssens, M.; Boiten, W. A.; van Drongelen, V.; Furio, L.; Vreeken, R. J.; Hovnanian, A.; Bouwstra, J. A. Intercellular skin barrier lipid composition and organization in Netherton syndrome patients. J. Invest. Dermatol. 2013.
35. van Smeden, J.; Janssens, M.; Kaye, E. C. J.; Caspers, P. J.; Lavrijsen, A. P.; Vreeken, R. J.; Bouwstra, J. A. The importance of free fatty acid chain length for the skin barrier function in atopic eczema patients Exp. Dermatol. 2014, 23, 45-52
36. Engelbrecht, T. N.; Schroeter, A.; Hauß, T.; Neubert, R. H. H. Lipophilic penetration enhancers and their impact to the bilayer structure of stratum corneum lipid model membranes: Neutron diffraction studies based on the example Oleic Acid Biochim. Biophys. Acta, Biomembr. 2011, 1808, 2798-2806
37. Mahjour, M.; Mauser, B. E.; Fawzi, M. B. Skin permeation enhancement effects of linoleic acid and azone on narcotic analgesics Int. J. Pharm. 1989, 56, 1-11
38. de Jager, M. W.; Gooris, G. S.; Ponec, M.; Bouwstra, J. A. Lipid mixtures prepared with well-defined synthetic ceramides closely mimic the unique stratum corneum lipid phase behavior J. Lipid Res. 2005, 46, 2649-2656
39. Wertz, P. W.; Downing, D. T. Epidermal lipids. In Physiology, Biochemistry, and Molecular Biology of the Skin; Goldsmith, L. A., Ed.; Oxford University Press: New York, 1991; pp 205-236.
40. Moore, D. J.; Rerek, M. E.; Mendelsohn, R. FTIR Spectroscopy studies of the conformational order and phase behavior of ceramides J. Phys. Chem. B 1997, 101, 8933-8940
41. Mendelsohn, R.; Liang, G. L.; Strauss, H. L.; Snyder, R. G. IR spectroscopic determination of gel state miscibility in long-chain phosphatidylcholine mixtures Biophys. J. 1995, 69, 1987-1998
42. Grayson, S.; Elias, P. M. Isolation and lipid biochemical characterization of stratum corneum membrane complexes: Implications for the cutaneous permeability barrier J. Investig. Dermatol. 1982, 78, 128-135
43. Hou, S. Y. E.; Mitra, A. K.; White, S. H.; Menon, G. K.; Ghadially, R.; Elias, P. M. Membrane structures in normal and essential fatty acid-deficient stratum corneum: Characterization by ruthenium tetroxide staining and X-ray diffraction J. Investig. Dermatol. 1991, 96, 215-223
44. Fartasch, M.; Bassukas, I. D.; Diepgen, T. L. Disturbed extruding mechanism of lamellar bodies in dry non-eczematous skin of atopics Br. J. Dermatol. 1992, 127, 221-227
45. McIntosh, T. J.; Stewart, M. E.; Downing, D. T. X-ray diffraction analysis of isolated skin lipids: Reconstitution of intercellular lipid domains Biochemistry 1996, 35, 3649-3653
46. Schröter, A.; Kessner, D.; Kiselev, M. A.; Hauß, T.; Dante, S.; Neubert, R. H. H. Basic nanostructure of stratum corneum lipid matrices based on ceramides [EOS] and [AP]: A neutron diffraction study Biophys. J. 2009, 97, 1104-1114
47. 2H NMR Int. J. Pharm. 2006, 307, 225-231
48. Rerek, M. E.; Van Wyck, D.; Mendelsohn, R.; Moore, D. J. FTIR spectroscopic studies of lipid dynamics in phytosphingosine ceramide models of the stratum corneum lipid matrix Chem. Phys. Lipids 2005, 134, 51-58
49. Basse, L. H.; Groen, D.; Bouwstra, J. A. Permeability and lipid organization of a novel psoriasis stratum corneum substitute Int. J. Pharm. 2013, 457, 275-282
50. Školová, B.; Janůšová, B.; Zbytovská, J.; Gooris, G.; Bouwstra, J.; Slepička, P.; Berka, P.; Roh, J.; Palát, K.; Hrabálek, A.; Vávrová, K. Ceramides in the skin lipid membranes: Length matters Langmuir 2013, 29, 15624-15633
51. van Smeden, J.; Janssens, M.; Gooris, G. S.; Bouwstra, J. A. The important role of stratum corneum lipids for the cutaneous barrier function Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2014, 1841, 295-313
52. Elias, P. M. Lipid abnormalities and lipid-based repair strategies in atopic dermatitis Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2014, 1841, 323-330
53. Jager, M.; Groenink, W.; Bielsa i Guivernau, R.; Andersson, E.; Angelova, N.; Ponec, M.; Bouwstra, J. A novel in vitro percutaneous penetration model: Evaluation of barrier properties with p -aminobenzoic acid and two of its derivatives Pharm. Res. 2006, 23, 951-960
54. Bouwstra, J. A.; Gooris, G. S.; Cheng, K.; Weerheim, A.; Bras, W.; Ponec, M. Phase behavior of isolated skin lipids J. Lipid Res. 1996, 37, 999-1011
55. Bouwstra, J. A.; Gooris, G. S.; Dubbelaar, F. E. R.; Ponec, M. Phase behavior of lipid mixtures based on human ceramides: Coexistence of crystalline and liquid phases J. Lipid Res. 2001, 42, 1759-1770
56. Johnson, M. E.; Blankschtein, D.; Langer, R. Evaluation of solute permeation through the stratum corneum: Lateral bilayer diffusion as the primary transport mechanism J. Pharm. Sci. 1997, 86, 1162-1172
57. Boddé, H. E.; van den Brink, I.; Koerten, H. K.; de Haan, F. H. N. Visualization of in vitro percutaneous penetration of mercuric chloride; Transport through intercellular space versus cellular uptake through desmosomes J. Controlled Release 1991, 15, 227-236
58. Hansen, S.; Naegel, A.; Heisig, M.; Wittum, G.; Neumann, D.; Kostka, K.-H.; Meiers, P.; Lehr, C.-M.; Schaefer, U. The role of corneocytes in skin transport revised-A combined computational and experimental approach Pharm. Res. 2009, 26, 1379-1397
59. Naik, A.; Pechtold, L. A. R. M.; Potts, R. O.; Guy, R. H. Mechanism of oleic acid-induced skin penetration enhancement in vivo in humans J. Controlled Release 1995, 37, 299-306
60. Pathan, I. B.; Setty, C. M. Chemical penetration enhancers for transdermal drug delivery systems Trop. J. Pharm. Res. 2009, 8, 173-179