The permeability enhancing mechanism of DMSO in ceramide bilayers simulated by molecular dynamics

Biophysical Journal

Volumn 93, Issue 6, 2007, Pages 2056-2068

  Notman, Rebecca ^a   Den Otter, Wouter K ^b   Noro, Massimo G ^c   Briels, W J ^b   Anwar, Jamshed ^d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TWENTE   (Netherlands)

^c UNILEVER RESEARCH   (United Kingdom)

^d UNIVERSITY OF BRADFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; DIMETHYL SULFOXIDE;

ARTICLE; CHEMICAL STRUCTURE; DENSITY; ELASTICITY; HYDROGEN BOND; LIPID BILAYER; LIQUID CRYSTAL; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS; PHASE TRANSITION; SKIN PENETRATION; STRATUM CORNEUM; TEMPERATURE DEPENDENCE;

EID: 34548714202     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.104703     Document Type: Article

References (61)

1. Elias, P. M. 1983. Epidermal lipids, barrier function, and desquamation. J. Invest. Dermatol. 80(Suppl. 6):44-49.
2. Williams, A. C. 2003. Theoretical aspects of transdermal drug delivery. In Transdermal and Topical Drug Delivery. T. K. Ghosh, W. Pfister, and S. I. Yum, editors. Pharmaceutical Press: From Theory to Clinical Practice, London. 27-49.
3. Barry, B. W. 1983. Dermatological Formulations: Percutaneous Absoprtion. Informa Healthcare, London.
4. Williams, A. C., and B. W. Barry. 2004. Penetration enhancers. Adv. Drug Del. Rev. 56:603-618.
5. Williams, M. L., and P. M. Elias. 1987. The extracellular-matrix of stratum-corneum: role of lipids in normal and pathological function. CRC Critical Reviews in Therapeutic Drug Carrier Systems. 3:95-122.
6. Wertz, P. W., and D. T. Downing. 1996. The nature of the epidermal barrier: biochemical aspects. Adv. Drug Del. Rev. 18:283-294.
7. Bouwstra, J. A., F. E. R. Dubbelaar, G. S. Gooris, and M. Ponec. 2000. The lipid organisation in the skin barrier. Acta Derm. Venereol. 80(Suppl. 208):23-30.
8. Bouwstra, J. A., G. S. Gooris, M. A. Salomons-de Vries, J. A. 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. Int. J. Pharm. 84:205-216.
9. Pilgram, G. S. K., 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.
10. Bommannan, D., R. O. Potts, and R. H. Guy. 1990. Examination of stratum corneum barrier function in vivo by infrared spectroscopy. J. Invest. Dermatol. 95:403-408.
11. Ongpipattanakul, B., M. L. Francoeur, and R. O. Potts. 1994. Polymorphism in stratum corneum lipids. Biochim. Biophys. Acta. 1190:115-122.
12. Hauser, J. M. L., B. M. Buehrer, and R. M. Bell. 1994. Role of ceramide in mitogenesis induced by exogenous sphingoid bases. J. Biol. Chem. 269:6803-6809.
13. Perry, D. K., and Y. A. Hannun. 1998. The role of ceramide in cell signaling. Biochim. Biophys. Acta. 1436:233-243.
14. Kronke, M. 1999. Biophysics of ceramide signaling: interaction with proteins and phase transition of membranes. Chem. Phys. Lipids. 101:109-121.
15. Moore, D. J., M. E. Rerek, and R. Mendelsohn. 1997. FTIR spectroscopy studies of the conformational order and phase behavior of ceramides. J. Phys. Chem. B. 101:8933-8940.
16. Moore, D. J., M. E. Rerek, and R. Mendelsohn. 1997. Lipid domains and orthorhombic phases in model stratum corneum: evidence from Fourier transform infrared spectroscopy studies. Biochem. Biophys. Res. Commun. 231:797-801.
17. Pascher, I. 1976. Molecular arrangements in sphingolipids: conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability. Biochim. Biophys. Acta. 455:433-451.
18. Moore, D. J., M. E. Rerek, and R. Mendelsohn. 1999. Role of ceramides 2 and 5 in the structure of the stratum corneum lipid barrier. Int. J. Cosmet. Sci. 21:353-368.
19. Moore, D. J., and M. E. Rerek. 2000. Insights into the molecular organization of lipids in the skin barrier from infrared spectroscopy studies of stratum corneum lipid models. Acta Derm. Venereol. 80(Suppl. 208):16-22.
20. Carrer, D. C., S. Schreier, M. Patrito, and B. Maggio. 2006. Effects of a short-chain ceramide on bilayer domain formation, thickness, and chain mobililty: DMPC and asymmetric ceramide mixtures. Biophys. J. 90:2394-2403.
21. Shah, J., J. M. Atienza, R. I. Duclos, A. V. Rawlings, Z. Dong, and G. G. Shipley. 1995. Structual and thermotropic properties of synthetic C16:0 (palmitoyl) ceramide: effect of hydration. J. Lipid Res. 36:1936-1944.
22. Shah, J., J. M. Atienza, A. V. Rawlings, and G. G. Shipley. 1995. Physical properties of ceramides: effect of fatty acid hydroxylation. J. Lipid Res. 36:1945-1955.
23. Rerek, M. E., H.-C. Chen, B. Markovic, D. Van Wyck, P. Garidel, R. Mendelsohn, and D. J. Moore. 2001. Phytosphingosine and sphingosine ceramide headgroup hydrogen bonding: structural insights through thermotropic hydrogen/deuterium exchange. J. Phys. Chem. B. 105:9355-9362.
24. de Jager, M. W., G. S. Gooris, I. P. Dolbnya, W. Bras, M. Ponec, and J. A. Bouwstra. 2003. The phase behaviour of skin lipid mixtures based on synthetic ceramides. Chem. Phys. Lipids. 124:123-134.
25. Sot, J., F. J. Aranda, M.-I. Collado, F. M. Goni, and A. Alonso. 2005. Different effects of long- and short-chain ceramides on the gel-fluid and lamellar-hexagonal transitions of phospholipids: a calorimetric, NMR, and x-ray diffraction study. Biophys. J. 88:3368-3380.
26. Scheffer, L., I. Solomonov, M. J. Weygand, K. Kjaer, L. Leiserowitz, and L. Addadi. 2005. Structure of cholesterol/ceramide monolayer mixtures: implications to the molecular organization of lipid rafts. Biophys. J. 88:3381-3391.
27. Brockman, H. L., M. M. Momsen, R. E. Brown, L. He, J. Chun, H.-S. Byun, and R. Bittman. 2004. The 4,5-double bond of ceramide regulates its dipole potential, elastic properties, and packing behavior. Biophys. J. 87:1722-1731.
28. Walker, R. B., and E. W. Smith. 1996. The role of percutaneous penetration enhancers. Adv. Drug Del. Rev. 18:295-301.
29. Hadgraft, J. 1999. Passive enhancement strategies in topical and transdermal drug delivery. Int. J. Pharm. 184:1-6.
30. Karande, P., A. Jain, and S. Mitragotri. 2004. Discovery of transdermal penetration enhancers by high-throughput screening. Nat. Biotechnol. 22:192-197.
31. Smith, E. W., and H. I. Maiback. 2005. Percutaneous Enhancers, 2nd ed. CRC Press, Boca Raton, FL.
32. Barry, B. W. 1987. Mode of action of penetration enhancers in human skin. J. Controlled Release. 6:85-97.
33. Anigbogu, A. N. C., A. C. Williams, B. W. Barry, and H. G. M. Edwards. 1995. Fourier transform Raman spectroscopy of interactions between the penetration enhancer dimethyl sulfoxide and human stratum corneum. Int. J. Pharm. 125:265-282.
34. Oertel, R. P. 1977. Protein conformational changes induced in human stratum corneum by organic sulfoxides: an infrared spectroscopic investigation. Biopolymers. 16:2329-2345.
35. Anchordoguy, T. J., J. F. Carpenter, J. H. Crowe, and L. M. Crowe. 1992. Temperature-dependent perturbation of phospholipid bilayers by dimethylsulfoxide. Biochim. Biophys. Acta. 1104:117-122.
36. Yu, Z. W., and P. J. Quinn. 1998. The modulation of membrane structure and stability by dimethyl sulphoxide (review). Mol. Membr. Biol. 15:59-68.
37. Rall, W. F., and G. M. Fahy. 1985. Ice-free cryopreservation of mouse embryos at - 196°C by vitrification. Nature. 313:573-575.
38. Kasai, M. 2002. Advances in the cryopreservation of mammalian oocytes and embryos: development of ultrarapid vitrification. Reprod. Med. Biol. 1:1-9.
39. Smondyrev, A. M., and M. L. Berkowitz. 1999. Molecular dynamics simulation of DPPC bilayer in DMSO. Biophys. J. 76:2472-2478.
40. Sum, A. K., and J. J. de Pablo. 2003. Molecular simulation study on the influence of dimethylsulfoxide on the structure of phospholipid bilayers. Biophys. J. 85:3636-3645.
41. Notman, R., M. Noro, B. O'Malley, and J. Anwar. 2006. Molecular basis for dimethylsulfoxide (DMSO) action on lipid membranes. J. Am. Chem. Soc. 128:13982-13983.
42. Höltje, M., T. Forster, B. Brandt, T. Engels, W. von Rybinski, and H.-D. Holtje. 2001. Molecular dynamics simulations of stratum corneum lipid models: fatty acids and cholesterol. Biochim. Biophys. Acta. 1511:156-167.
43. Anishkin, A., S. Sukharev, and M. Colombini. 2006. Searching for the molecular arrangement of transmembrane ceramide channels. Biophys. J. 90:2414-2426.
44. Pandit, S. A., and H. L. Scott. 2006. Molecular-dynamics simulation of a ceramide bilayer. J. Chem. Phys. 124:014708.
45. Berger, O., O. Edholm, and F. Jahnig. 1997. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72:2002-2013.
46. Mombelli, E., R. Morris, W. Taylor, and F. Fraternali. 2003. Hydrogen-bonding propensities of sphingomyelin in solution and in a bilayer assembly: a molecular dynamics study. Biophys. J. 84:1507-1517.
47. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, and W. F. Hermans. 1981. Interaction models for water in relation to protein hydration. In Intermolecular Forces. B. Pullman, editor. D. Reidel Publishing, Dordrecht, The Netherlands. 331-342.
48. Bordat, P., J. Sacristan, D. Reith, S. Girard, A. Glattli, and F. Muller-Plathe. 2003. An improved dimethyl sulfoxide force field for molecular dynamics simulations. Chem. Phys. Lett. 374:201-205.
49. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: A package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
50. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of the equations of motion for a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23:327-341.
51. Patra, M., M. Karttunen, M. T. Hyvonen, E. Falck, P. Lindqvist, and I. Vattulainen. 2003. Molecular dynamics simulations of lipid bilayers: major artifacts due to truncating electrostatic interactions. Biophys. J. 84:3636-3645.
52. Wohlert, J., and O. Edholm. 2004. The range and shielding of dipole-dipole interactions in phospholipid bilayers. Biophys. J. 87:2433-2445.
53. Chen, H.-C., R. Mendelsohn, M. E. Rerek, and D. J. Moore. 2000. Fourier transform infrared spectroscopy and differential scanning calorimetry studies of fatty acid homogeneous ceramide 2. Biochim. Biophys. Acta. 1468:293-303.
54. Dahlen, B., and I. Pascher. 1979. Molecular arrangements in sphingolipids. Thermotropic phase behaviour of tetracosanoylphytosphingosine. Chem. Phys. Lipids. 24:119-133.
55. Van der Spoel, D., E. Lindahl, B. Hess, A. R. van Buuren, E. Apol, P. J. Meulenhoff, D. P. Tieleman, A. L. T. M. Sijbers, K. A. Feenstra, R. van Drunen, and H. J. C. Berendsen. 2004. Gromacs User Manual version 3.2. http://www.gromacs.org/.
56. Herce, H. D., and A. E. Garcia. 2006. Correction of apparent finite size effects in the area per lipid of lipid membrane simulations. J. Chem. Phys. 125:224711.
57. Rand, R. P., and V. A. Parsegian. 1989. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta. 988:351-376.
58. Chiu, S. W., S. Vasudevan, E. Jakobsson, R. J. Mashl, and H. L. Scott. 2003. Structure of sphingomyelin bilayers: a simulation study. Biophys. J. 85:3624-3635.
59. Dahlen, B., and I. Pascher. 1972. Molecular arrangements in sphingolipids. Crystal structure of N-tetracosanoylphytosphingosine. Acta Crystallogr., Sect. B: Struct. Crystallogr. Cryst. Chem. 28:2396-2404.
60. Pascher, I., and S. Sundell. 1992. Molecular arrangements in sphingolipids: crystal structure of the ceramide N-(2D,3D-dihydroxyoctadecanoyl) -phytosphingosine. Chem. Phys. Lipids. 61:79-86.
61. Kligman, A. M. 1965. Topical pharmacology and toxicology of dimethyl sulphoxide. 1. JAMA. 193:796-804.