Direct visualization of lipid domains in human skin stratum corneum's lipid membranes: Effect of pH and temperature

Biophysical Journal

Volumn 93, Issue 9, 2007, Pages 3142-3155

  Plasencia, I ^a   Norlen L ^b,c   Bagatolli, Luis A ^a,d  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b KAROLINSKA INSTITUTE   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d Dept of Biochemistry and Molecular Biology   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; CHOLESTEROL; FATTY ACID;

ARTICLE; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; FLUORESCENCE SPECTROSCOPY; HUMAN; HUMAN TISSUE; LIPID MEMBRANE; MEMBRANE STRUCTURE; PH; SKIN TEMPERATURE; STRATUM CORNEUM; TEMPERATURE;

EID: 36049033182     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.096164     Document Type: Article

References (80)

1. Blank, I. H. 1952. Factors which influence the water content of the stratum corneum. J. Invest. Dermatol. 18:433-440.
2. Forslind, B. 1994. A domain mosaic model of the skin barrier. Acta Derm. Venereol. 74:1-6.
3. Michaels, A. S., S. K. Chandrasekaran, and J. E. Shaw. 1975. Drug permeation through human skin: theory and in vitro experimental measurements. AIChE J. 21:985-996.
4. Norlén, L. 2001. Skin barrier structure and function: the single gel phase model. J. Invest. Dermatol. 117:830-836.
5. Norlén, L., A. Al-Amoudi, and J. Dubochet. 2003. A cryotransmission electron microscopy study of skin barrier formation. J. Invest. Dermatol. 120:555-560.
6. Bouwstra, J. A., F. E. Dubbelaar, G. S. Gooris, and M. Ponec. 2000. The lipid organisation in the skin barrier. Acta Derm. Venereol. Suppl. (Stockh.). 208:23-30.
7. McIntosh, T. J. 2003. Organization of skin stratum corneum extracellular lamellae: diffraction evidence for asymmetric distribution of cholesterol. Biophys. J. 85:1675-1681.
8. Bouwstra, J. A., G. S. Pilgram, and M. Ponec. 2002. Does the single gel phase exist in stratum corneum? J. Invest. Dermatol. 118:897-898; author reply 899-901.
9. Norlén, L. 2002. Does the single gel phase exist in stratum corneum? Reply. J. Invest. Dermatol. 118:897-898; author reply 899-901.
10. Norlén, L., I. Plasencia, A. Simonsen, and P. Descouts. 2007. Human stratum corneum lipid organization as observed by atomic force microscopy on Langmuir-Blodgett films. J. Struct. Biol. 158:386-400.
11. Wertz, P. W., and B. B. Michniak. 2000. Sebum. In Cosmeceuticals: Drugs vs. Cosmetics. P. Elsner and H. I. Maibach, editors. Marcel Dekker, New York. 45-46.
12. Norlén, L., I. Nicander, A. Lundsjo, T. Cronholm, and B. Forslind. 1998. A new HPLC-based method for the quantitative analysis of inner stratum corneum lipids with special reference to the free fatty acid fraction. Arch. Dermatol. Res. 290:508-516.
13. Wertz, P., and L. Norlén. 2003. "Confidence intervals" for the "true" lipid composition of the human skin barrier? In Skin, Hair, and Nails. Structure and Function. B. Forslind and M. Lindberg, editors. Marcel Dekker. 85-106.
14. Wertz, P. W., D. C. Swartzendruber, K. C. Madison, and D. T. Downing. 1987. Composition and morphology of epidermal cyst lipids. J. Invest. Dermatol. 89:419-425.
15. Farwanah, H., J. Wohlrab, R. H. Neubert, and K. Raith. 2005. Profiling of human stratum corneum ceramides by means of normal phase LC/ APCI-MS. Anal. Bioanal. Chem. 383:632-637.
16. Vietzke, J. P., O. Brandt, D. Abeck, C. Rapp, M. Strassner, V. Schreiner, and U. Hintze. 2001. Comparative investigation of human stratum corneum ceramides. Lipids. 36:299-304.
17. Norlén, L., I. Nicander, B. Lundh Rozell, S. Ollmar, and B. Forslind. 1999a. Inter- and intra-individual differences in human stratum corneum lipid content related to physical parameters of skin barrier function in vivo. J. Invest. Dermatol. 112:72-77.
18. Bouwstra, J., G. S. Gooris, M. A. Salmon-de-Vries, J. van der Spek, and W. Bras. 1992. Structure of human stratum corneum as a function of temperature and hydration: a wide-angle x-ray diffraction study. Inter. J. Pharmaceut. 84:205-216.
19. Garson, J. C., J. Doucet, J. L. Leveque, and G. Tsoucaris. 1991. Oriented structure in human stratum corneum revealed by x-ray diffraction. J. Invest. Dermatol. 96:43-49.
20. Goldsmith, L. A., and H. P. Baden. 1970. Uniquely oriented epidermal lipid. Nature. 225:1052-1053.
21. Hatta, I., N. Ohta, K. Inoue, and N. Yagi. 2006. Coexistence of two domains in intercellular lipid matrix of stratum corneum. Biochim. Biophys. Acta. 1758:1830-1836.
22. Swanbeck, G. 1959. Macromolecular organization of epidermal keratin: an x-ray diffraction study of the horny layer from normal, ichthyotic and psoriatic skin. Acta Derm. Venereol. Suppl. (Stockh.). 39(Suppl. 43):1-37.
23. White, S. H., D. Mirejovsky, and G. I. King. 1988. Structure of lamellar lipid domains and corneocyte envelopes of murine stratum corneum. An x-ray diffraction study. Biochemistry. 27:3725-3732.
24. Wilkes, G. L., A. L. Nguyen, and R. Wildnauer. 1973. Structure-property relations of human and neonatal rat stratum corneum. I. Thermal stability of the crystalline lipid structure as studied by x-ray diffraction and differential thermal analysis. Biochim. Biophys. Acta. 304:265-275.
25. Pilgram, G. S., A. M. Engelsma-van Pelt, J. A. Bouwstra, and H. K. Koerten. 1999. Electron diffraction provides new information on human stratum corneum lipid organization studied in relation to depth and temperature. J. Invest. Dermatol. 113:403-409.
26. Bouwstra, J. A., G. S. Gooris, J. A. van der Spek, and W. Bras. 1991. Structural investigations of human stratum corneum by small-angle x-ray scattering. J. Invest. Dermatol. 97:1005-1012.
27. Swartzendruber, D. C., P. W. Wertz, D. J. Kitko, K. C. Madison, and D. T. Downing. 1989. Molecular models of the intercellular lipid lamellae in mammalian stratum corneum. J. Invest. Dermatol. 92:251-257.
28. Al-Amoudi, A., J. Dubochet, and L. Norlén. 2005. Nanostructure of the epidermal extracellular space as observed by cryo-electron microscopy of vitreous sections of human skin. J. Invest. Dermatol. 124:764-777.
29. Charalambopoulos, G. C., T. A. Striotis, T. Hauss, A. K. Stubos, and N. K. Kanellopoulos. 2004. Structural alterations of fully hydrated human stratum corneum. Physica B (Amsterdam). 350:e603-e606.
30. Hernquist, L. 1984. Polymorphism of fats. PhD thesis. Lund University, Lund, Sweden.
31. Larsson, K. 1994. Lipids: molecular organisation, physical functions and technical applications. The Oily Press, Dundee, Scotland.
32. Carruthers, A., and D. L. Melchior. 1983. Studies of the relationship between bilayer water permeability and bilayer physical state. Biochemistry. 22:5797-5807.
33. Naik, A., and R. H. Guy. 1997. Infrared spectroscopy and differential scanning calorimetric investigations of the stratum corneum barrier function. In Mechanisms of Transdermal Drug Delivery. R. O. Potts and R. H. Guy, editors. Marcel Dekker, New York. 87-162.
34. Ananthapadmanabhan, K. P., A. Lips, C. Vincent, F. Meyer, C. Caso, A. Johnson, K. Subramanyan, M. Vetharmuthu, G. Rattinger, and D. J. Moore. 2003. pH-induced alterations in stratum corneum properties. Int. J. Cosm. Sci. 25:103-112.
35. Behne, M. J., N. P. Barry, K. M. Hanson, I. Aronchik, R. W. Clegg, E. Gratton, K. Feingold, W. M. Holleran, P. M. Elias, and T. M. Mauro. 2003. Neonatal development of the stratum corneum pH gradient: localization and mechanisms leading to emergence of optimal barrier function. J. Invest. Dermatol. 120:998-1006.
36. Fluhr, J. W., M. Mao-Qiang, B. E. Brown, J. P. Hachem, D. G. Moskowitz, M. Demerjian, M. Haftek, G. Serre, D. Crumrine, T. M. Mauro, P. M. Elias, and K. R. Feingold. 2004. Functional consequences of a neutral pH in neonatal rat stratum corneum. J. Invest. Dermatol. 123:140-151.
37. Hachem, J. P., D. Crumrine, J. Fluhr, B. E. Brown, K. R. Feingold, and P. M. Elias. 2003. pH directly regulates epidermal permeability barrier homeostasis, and stratum corneum integrity/cohesion. J. Invest. Dermatol. 121:345-353.
38. Hachem, J. P., M. Q. Man, D. Crumrine, Y. Uchida, B. E. Brown, V. Rogiers, D. Roseeuw, K. R. Feingold, and P. M. Elias. 2005. Sustained serine proteases activity by prolonged increase in pH leads to degradation of lipid processing enzymes and profound alterations of barrier function and stratum corneum integrity. J. Invest. Dermatol. 125:510-520.
39. Eberlein-Konig, B., T. Schafer, J. Huss-Marp, U. Darsow, M. Mohrenschlager, O. Herbert, D. Abeck, U. Kramer, H. Behrendt, and J. Ring. 2000. Skin surface pH, stratum corneum hydration, transepidermal water loss and skin roughness related to atopic eczema and skin dryness in a population of primary school children. Acta Derm. Venereol. 80:188-191.
40. Öhman, H., and A. Vahlquist. 1998. The pH gradient over the stratum corneum differs in X-linked recessive and autosomal dominant ichthyosis: a clue to the molecular origin of the "acid skin mantle"? J. Invest. Dermatol. 111:674-677.
41. Schmid-Wendtner, M. H., and H. C. Korting. 2006. The pH of the skin surface and its impact on the barrier function. Skin Pharmacol. Physiol. 19:296-302.
42. Werner, Y., and M. Lindberg. 1985. Transepidermal water loss in dry and clinically normal skin in patients with atopic dermatitis. Acta Derm. Venereol. 65:102-105.
43. Cunico, R. L., H. I. Maibach, H. Khan, and E. Bloom. 1977. Skin barrier properties in the newborn. Transepidermal water loss and carbon dioxide emission rates. Biol. Neonate. 32:177-182.
44. Berg, R. W., M. C. Milligan, and F. C. Sarbaugh. 1994. Association of skin wetness and pH with diaper dermatitis. Pediatr. Dermatol. 11:18-20.
45. Nilsson, G. E. 1977. On the measurements of evaporative water loss - methods and clinical applications. PhD thesis. Dept. of Medical Engineering, University of Linköping, Linköping, Sweden.
46. Norlén, L., J. Engblom, M. Andersson, and B. Forslind. 1999. A new computer-based evaporimeter system for rapid and precise measurements of water diffusion through stratum corneum in vitro. J. Invest. Dermatol. 113:533-540.
47. Denda, M., J. Hosoi, and Y. Asida. 2000. Visual imaging of ion distribution in human epidermis. Biochem. Biophys. Res. Commun. 272:134-137.
48. Öhman, H., and A. Vahlquist. 1994. In vivo studies concerning a pH gradient in human stratum corneum and upper epidermis. Acta Derm. Venereol. 74:375-379.
49. Hanson, K. M., M. J. Behne, N. P. Barry, T. M. Mauro, E. Gratton, and R. M. Clegg. 2002. Two-photon fluorescence lifetime imaging of the skin stratum corneum pH gradient. Biophys. J. 83:1682-1690.
50. Ouimet, J., S. Croft, C. Pare, J. Katsaras, and M. Lafleur. 2003. Modulation of the polymorphism of the palmitic acid/cholesterol system by the pH. Langmuir. 19:1089-1097.
51. Keller, D., N. B. Larsen, I. M. Moller, and O. G. Mouritsen. 2005. Decoupled phase transitions and grain-boundary melting in supported phospholipid bilayers. Phys. Rev. Lett. 94:025701.
52. Bouwstra, J. A., G. S. Gooris, F. E. Dubbelaar, A. M. Weerheim, and M. Ponec. 1998. pH, cholesterol sulfate, and fatty acids affect the stratum corneum lipid organization. J. Investig. Dermatol. Symp. Proc. 3:69-74.
53. Bagatolli, L. A. 2006. To see or not to see: lateral organization of biological membranes and fluorescence microscopy. Biochim. Biophys. Acta. 1758:1541-1556.
54. Parasassi, T., G. De Stasio, A. d'Ubaldo, and E. Gratton. 1990. Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys. J. 57:1179-1186.
55. Fidorra, M., L. Duelund, C. Leidy, A. Simonsen, and L. A. Bagatolli. 2006. Absence of fluid-ordered/fluid-disordered phase coexistence in ceramide/POPC mixtures containing cholesterol. Biophys. J. 90:4437-4451.
56. Golden, G. M., D. B. Guzek, R. R. Harris, J. E. McKie, and R. O. Potts. 1986. Lipid thermotropic transitions in human stratum corneum. J. Invest. Dermatol. 86:255-259.
57. Van Duzee, B. F. 1975. Thermal analysis of human stratum corneum. J. Invest. Dermatol. 65:404-408.
58. Gay, C. L., R. H. Guy, G. M. Golden, V. H. Mak, and M. L. Francoeur. 1994. Characterization of low-temperature (i.e., < 65 degrees C) lipid transitions in human stratum corneum. J. Invest. Dermatol. 103:233-239.
59. Babita, K., V. Kumar, V. Rana, S. Jain, and A. K. Tiwary. 2006. Thermotropic and spectroscopic behavior of skin: relationship with percutaneous permeation enhancement. Curr. Drug Des. Deliv. 3:95-113.
60. Parasassi, T., and E. Gratton. 1995. Membrane lipid domains and dynamics as detected by Laurdan fluorescence. J. Fluoresc. 2:167-174.
61. Bagatolli, L. A. 2003. Thermotropic behavior of lipid mixtures studied at the level of single vesicles: giant unilamellar vesicles and two-photon excitation fluorescence microscopy. Methods Enzymol. 367:233-253.
62. Bagatolli, L. A., and E. Gratton. 2001. Direct observation of lipid domains in freestanding bilayers using two-photon excitation fluorescence microscopy. J. Fluoresc. 11:141-160.
63. Bagatolli, L. A., and E. Gratton. 2000. A correlation between lipid domain shape and binary phospholipid mixture composition in free standing bilayers: a two-photon fluorescence microscopy study. Biophys. J. 79:434-447.
64. Mathivet, L., S. Cribier, and P. F. Devaux. 1996. Shape change and physical properties of giant phospholipid vesicles prepared in the presence of an AC electric field. Biophys. J. 70:1112-1121.
65. Bernardino de la Serna, J., J. Perez-Gil, A. C. Simonsen, and L. A. Bagatolli. 2004. Cholesterol rules: direct observation of the coexistence of two fluid phases in native pulmonary surfactant membranes at physiological temperatures. J. Biol. Chem. 279:40715-40722.
66. Dietrich, C., L. A. Bagatolli, Z. N. Volovyk, N. L. Thompson, M. Levi, K. Jacobson, and E. Gratton. 2001. Lipid rafts reconstituted in model membranes. Biophys. J. 80:1417-1428.
67. Saenz, A., O. Canadas, L. A. Bagatolli, M. E. Johnson, and C. Casals. 2006. Physical properties and surface activity of surfactant-like membranes containing the cationic and hydrophobic peptide KL. FEBS J. 273:2515-2527.
68. ten Grotenhuis, E., R. A. Demel, M. Ponec, D. R. Boer, J. C. van Miltenburg, and J. A. Bouwstra. 1996. Phase behavior of stratum corneum lipids in mixed Langmuir-Blodgett monolayers. Biophys. J. 71:1389-1399.
69. McIntosh, T. J., M. E. Stewart, and D. T. Downing. 1996. X-ray diffraction analysis of isolated skin lipids: reconstitution of intercellular lipid domains. Biochemistry. 35:3649-3653.
70. Gooris, G. S., and J. A. Bouwstra. 2007. Infrared spectroscopic study of stratum corneum model membranes prepared from human ceramides, cholesterol, and fatty acids. Biophys. J.92:2785-2795.
71. Glombitza, B., and C. C. Muller-Goymann. 2002. Influence of different ceramides on the structure of in vitro model lipid systems of the stratum corneum lipid matrix. Chem. Phys. Lipids. 117:29-44.
72. Bouwstra, J. A., and M. Ponec. 2006. The skin barrier in healthy and diseased state. Biochim. Biophys. Acta. 1758:2080-2095.
73. Bouwstra, J. A., P. L. Honeywell-Nguyen, G. S. Gooris, and M. Ponec. 2003. Structure of the skin barrier and its modulation by vesicular formulations. Prog. Lipid Res. 42:1-36.
74. Merkel, R., E. Sackmann, and E. Evans. 1989. Molecular friction and epitactic coupling between monolayers in supported bilayers. J. Phys. France. 50:1535-1555.
75. a of the fatty acids within ordered mixtures of model human stratum corneum lipids. Pharm. Res. 12:1614-1617.
76. Montes, L. R., M. B. Ruiz-Arguello, F. M. Goni, and A. Alonso. 2002. Membrane restructuring via ceramide results in enhanced solute efflux. J. Biol. Chem. 277:11788-11794.
77. Papahadjopoulos, D., K. Jacobson, S. Nir, and T. Isac. 1973. Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol. Biochim. Biophys. Acta. 311:330-348.
78. Ambroggio, E. E., F. Separovic, J. H. Bowie, G. D. Fidelio, and L. A. Bagatolli. 2005. Direct visualization of membrane leakage induced by the antibiotic peptides: maculatin, citropin, and aurein. Biophys. J. 89:1874-1881.
79. Simonetti, O., A. J. Hoogstraate, W. Bialik, J. A. Kempenaar, A. H. Schrijvers, H. E. Bodde, and M. Ponec. 1995. Visualization of diffusion pathways across the stratum corneum of native and in-vitro-reconstructed epidermis by confocal laser scanning microscopy. Arch. Dermatol. Res. 287:465-473.
80. Forslind, B. 1995. The skin: upholder of physiological homeostasis. A physiological and (bio) physical study program. Thromb. Res. 80:1-22.