The role of sphingolipid metabolism in cutaneous permeabilitybarrier formation

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 3, 2014, Pages 441-452

  Breiden, Bernadette ^a   Sandhoff, Konrad ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Acylceramide; Ceramide; Glucosylceramide; Sphingomyelin; Stratum corneum; Ultra long chain fatty acid

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A12; ACETYL COENZYME A; ALDEHYDE; ALDEHYDE DEHYDROGENASE; CERAMIDE; CHOLESTEROL; COENZYME A; DIACYLGLYCEROL; DIACYLGLYCEROL ACYLTRANSFERASE 2; FATTY ACID SYNTHASE; FATTY ACID TRANSPORTER 4; FATTY ALCOHOL; GLUCOSYLCERAMIDE; GLUCOSYLTRANSFERASE; GLYCOSPHINGOLIPID; HYDROLASE; LACTOSYLCERAMIDE; LINOLEIC ACID; LONG CHAIN FATTY ACID; MALONYL COENZYME A; PALMITOYL COENZYME A; PROSAPOSIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SPHINGANINE; SPHINGOLIPID; SPHINGOLIPID ACTIVATOR PROTEIN; SPHINGOMYELIN; ULTRA LONG CHAIN FATTY ACID; UNCLASSIFIED DRUG; VERY LONG CHAIN FATTY ACID;

ACYLATION; ATOPIC DERMATITIS; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL MEMBRANE; CELL ORGANELLE; CELL TYPE; CULTURE MEDIUM; CYTOSOL; DEGRADATION; DESICCATION; DESQUAMATION; EPIDERMIS; EXOCYTOSIS; EXTRACELLULAR SPACE; GESTATIONAL AGE; GLYCOSYLATION; GOLGI COMPLEX; HUMAN; HYDROLYSIS; HYDROXYLATION; HYPERKERATOSIS; ICHTHYOSIS; IN VITRO STUDY; INTERCELLULAR SPACE; KERATINOCYTE; LAMELLAR BODY; LAMELLAR ICHTHYOSIS; LIPID ANALYSIS; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; LIPID METABOLISM; LIPIDOSIS; LIPOGENESIS; LOSS OF FUNCTION MUTATION; LYSOSOME; MISSENSE MUTATION; MITOCHONDRION; NEWBORN DEATH; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PERMEABILITY BARRIER; PH; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PSORIASIS VULGARIS; REFSUM DISEASE; RETINA MACULA DEGENERATION; REVIEW; RISK FACTOR; SEBACEOUS GLAND HYPERPLASIA; SECRETORY PATHWAY; SKIN PERMEABILITY; SKIN PROTECTION; SKIN WATER LOSS; STRATUM CORNEUM; WATER CONTENT; WATER LOSS; WATER PERMEABILITY;

MAMMALIA;

ACYLCERAMIDE; CERAMIDE; GLUCOSYLCERAMIDE; SPHINGOMYELIN; STRATUM CORNEUM; ULTRA LONG CHAIN FATTY ACID;

ANIMALS; EPIDERMIS; GLUCOSYLCERAMIDES; GLYCOSYLATION; GOLGI APPARATUS; HUMANS; INTRACELLULAR MEMBRANES; LINOLEIC ACID; LIPID METABOLISM; PERMEABILITY;

EID: 84896723076     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.08.010     Document Type: Review

References (151)

1. D. Downing Lipid and protein structures in the permeability barrier of mammalian epidermis J. Lipid Res. 33 1992 301 313
2. P.M. Elias, and G.K. Menon Structural and lipid biochemical correlates of the epidermal permeability barrier Adv. Lipid Res. 24 1991 1 26
3. J.A. Bouwstra, P.L. Honeywell-Nguyen, G.S. Gooris, and M. Ponec Structure of the skin barrier and its modulation by vesicular formulations Prog. Lipid Res. 42 2003 1 36 (Pubitemid 35418207)
4. M. Ponec, A. Weerheim, P. Lankhorst, and P. Wertz New acylceramide in native and reconstructed epidermis J. Invest. Dermatol. 120 2003 581 588 (Pubitemid 36344000)
5. K.J. Robson, M.E. Stewart, S. Michelsen, N.D. Lazo, and D.T. Downing 6-Hydroxy-4-sphingenine in human epidermal ceramides J. Lipid Res. 35 1994 2060 2068 (Pubitemid 24353078)
6. M.E. Stewart, and D.T. Downing The omega-hydroxyceramides of pig epidermis are attached to corneocytes solely through omega-hydroxyl groups J. Lipid Res. 42 2001 1105 1110 (Pubitemid 32645792)
7. R. t'Kindt, L. Jorge, E. Dumont, P. Couturon, F. David, P. Sandra, and K. Sandra Profiling and characterizing skin ceramides using reversed-phase liquid chromatography-quadrupole time-of-flight mass spectrometry Anal. Chem. 84 2012 403 411
8. J. van Smeden, L. Hoppel, R. van der Heijden, T. Hankemeier, R.J. Vreeken, and J.A. Bouwstra LC/MS analysis of stratum corneum lipids: ceramide profiling and discovery J. Lipid Res. 52 2011 1211 1221
9. S. Motta, M. Monti, S. Sesana, R. Caputo, S. Carelli, and R. Ghidoni Ceramide composition of the psoriatic scale Biochim. Biophys. Acta 1182 1993 147 151 (Pubitemid 23267037)
10. Y. Masukawa, H. Narita, E. Shimizu, N. Kondo, Y. Sugai, T. Oba, R. Homma, J. Ishikawa, Y. Takagi, T. Kitahara, Y. Takema, and K. Kita Characterization of overall ceramide species in human stratum corneum J. Lipid Res. 49 2008 1466 1476
11. E.M. Meier, D. Schummer, and K. Sandhoff Evidence for the presence of water within the hydrophobic core of membranes Chem. Phys. Lipids 55 1990 103 113 (Pubitemid 20261618)
12. R. Jennemann, M. Rabionet, K. Gorgas, S. Epstein, A. Dalpke, U. Rothermel, A. Bayerle, F. van der Hoeven, S. Imgrund, J. Kirsch, W. Nickel, K. Willecke, H. Riezman, H.J. Gröne, and R. Sandhoff Loss of ceramide synthase 3 causes lethal skin barrier disruption Hum. Mol. Genet. 21 2012 586 608
13. A. Steven, and P. Steinert Protein composition of cornified cell envelopes of epidermal keratinocytes J. Cell Sci. 107 1994 693 700 (Pubitemid 24072900)
14. L.N. Marekov, and P.M. Steinert Ceramides are bound to structural proteins of the human foreskin epidermal cornified cell envelope J. Biol. Chem. 273 1998 17763 17770 (Pubitemid 28355119)
15. J.V. Frei, and H. Sheldon A small granular component of the cytoplasm of keratinizing epithelia J. Biophys. Biochem. Cytol. 11 1961 719 724
16. A.G. Matoltsy, and P.F. Parakkal Membrane-coating granules of keratinizing epithelia J. Cell Biol. 24 1965 297 307
17. P.W. Wertz, D.T. Downing, R.K. Freinkel, and T.N. Traczyk Sphingolipids of the stratum corneum and lamellar granules of fetal rat epidermis J. Invest. Dermatol. 83 1984 193 195 (Pubitemid 14063907)
18. S. Grayson, A.G. Johnson-Winegar, B.U. Wintroub, R.R. Isseroff, E.H. Epstein Jr., and P.M. Elias Lamellar body-enriched fractions from neonatal mice: preparative techniques and partial characterization J. Invest. Dermatol. 85 1985 289 294 (Pubitemid 15248010)
19. Y. Zuo, D.Z. Zhuang, R. Han, G. Isaac, J.J. Tobin, M. McKee, R. Welti, J.L. Brissette, M.L. Fitzgerald, and M.W. Freeman ABCA12 maintains the epidermal lipid permeability barrier by facilitating formation of ceramide linoleic esters J. Biol. Chem. 283 2008 36624 36635
20. T. Yanagi, M. Akiyama, H. Nishihara, K. Sakai, W. Nishie, S. Tanaka, and H. Shimizu Harlequin ichthyosis model mouse reveals alveolar collapse and severe fetal skin barrier defects Hum. Mol. Genet. 17 2008 3075 3083
21. D.P. Kelsell, E.E. Norgett, H. Unsworth, M.T. Teh, T. Cullup, C.A. Mein, P.J. Dopping-Hepenstal, B.A. Dale, G. Tadini, P. Fleckman, K.G. Stephens, V.P. Sybert, S.B. Mallory, B.V. North, D.R. Witt, E. Sprecher, A.E. Taylor, A. Ilchyshyn, C.T. Kennedy, H. Goodyear, C. Moss, D. Paige, J.I. Harper, B.D. Young, I.M. Leigh, R.A. Eady, and E.A. O'Toole Mutations in ABCA12 underlie the severe congenital skin disease harlequin ichthyosis Am. J. Hum. Genet. 76 2005 794 803 (Pubitemid 40563101)
22. P.W. Wertz, and D.T. Downing Glycolipids in mammalian epidermis: structure and function in the water barrier Science 217 1982 1261 1262
23. G.M. Gray, R.J. White, and J.R. Majer 1-(3′-O-acyl)-beta-glucosyl- N-dihydroxypentatriacontadienoylsphingosine, a major component of the glucosylceramides of pig and human epidermis Biochim. Biophys. Acta 528 1978 127 137
24. P.A. Bowser, D.H. Nugteren, R.J. White, U.M. Houtsmuller, and C. Prottey Identification, isolation and characterization of epidermal lipids containing linoleic acid Biochim. Biophys. Acta 834 1985 419 428 (Pubitemid 15025250)
25. T. Doering, W.M. Holleran, A. Potratz, G. Vielhaber, P.M. Elias, K. Suzuki, and K. Sandhoff Sphingolipid activator proteins are required for epidermal permeability barrier formation J. Biol. Chem. 274 1999 11038 11045
26. T. Doering, R.L. Proia, and K. Sandhoff Accumulation of protein-bound epidermal glucosylceramides in beta-glucocerebrosidase deficient type 2 Gaucher mice FEBS Lett. 447 1999 167 170 (Pubitemid 29146079)
27. D. Khnykin, J.H. Miner, and F. Jahnsen Role of fatty acid transporters in epidermis: implications for health and disease Dermatoendocrinology 3 2011 53 61
28. M. Behne, Y. Uchida, T. Seki, P.O. de Montellano, P.M. Elias, and W.M. Holleran Omega-hydroxyceramides are required for corneocyte lipid envelope (CLE) formation and normal epidermal permeability barrier function J. Invest. Dermatol. 114 2000 185 192 (Pubitemid 30195993)
29. A. Shibaki, M. Akiyama, and H. Shimizu Novel ALDH3A2 heterozygous mutations are associated with defective lamellar granule formation in a Japanese family of Sjögren-Larsson syndrome J. Invest. Dermatol. 123 2004 1197 1199 (Pubitemid 39586847)
30. W.B. Rizzo, D. S'Aulis, M.A. Jennings, D.A. Crumrine, M.L. Williams, and P.M. Elias Ichthyosis in Sjögren-Larsson syndrome reflects defective barrier function due to abnormal lamellar body structure and secretion Arch. Dermatol. Res. 302 2010 443 451
31. D.G. Paige, N. Morse-Fisher, and J.I. Harper Quantification of stratum corneum ceramides and lipid envelope ceramides in the hereditary ichthyoses Br. J. Dermatol. 131 1994 23 27 (Pubitemid 24234283)
32. R.J. Sanders, R. Ofman, G. Dacremont, R.J. Wanders, and S. Kemp Characterization of the human omega-oxidation pathway for omega-hydroxy-very- long-chain fatty acids FASEB J. 22 2008 2064 2071 (Pubitemid 351811482)
33. D.H. Nugteren The enzymic chain elongation of fatty acids by rat-liver microsomes Biochim. Biophys. Acta 106 1965 280 290
34. A. Jakobsson, R. Westerberg, and A. Jacobsson Fatty acid elongases in mammals: their regulation and roles in metabolism Prog. Lipid Res. 45 2006 237 249
35. Y. Ohno, S. Suto, M. Yamanaka, Y. Mizutani, S. Mitsutake, Y. Igarashi, T. Sassa, and A. Kihara ELOVL1 production of C24 acyl-CoAs is linked to C24 sphingolipid synthesis Proc. Natl. Acad. Sci. U. S. A. 107 2010 18439 18444
36. J. Rogers, C. Harding, A. Mayo, J. Banks, and A. Rawlings Stratum corneum lipids: the effect of ageing and the seasons Arch. Dermatol. Res. 288 1996 765 770 (Pubitemid 26388135)
37. A.E. Leonard, S.L. Pereira, H. Sprecher, and Y.S. Huang Elongation of long-chain fatty acids Prog. Lipid Res. 43 2004 36 54 (Pubitemid 37433866)
38. W. Li, R. Sandhoff, M. Kono, P. Zerfas, V. Hoffmann, B.C. Ding, R.L. Proia, and C.X. Deng Depletion of ceramides with very long chain fatty acids causes defective skin permeability barrier function, and neonatal lethality in ELOVL4 deficient mice Int. J. Biol. Sci. 3 2007 120 128 (Pubitemid 46232773)
39. V. Vasireddy, Y. Uchida, N. Salem Jr., S.Y. Kim, M.N. Mandal, G.B. Reddy, R. Bodepudi, N.L. Alderson, J.C. Brown, H. Hama, A. Dlugosz, P.M. Elias, W.M. Holleran, and R. Ayyagari Loss of functional ELOVL4 depletes very long-chain fatty acids (> or = C28) and the unique omega-O-acylceramides in skin leading to neonatal death Hum. Mol. Genet. 16 2007 471 482 (Pubitemid 46522611)
40. T. Sassa, Y. Ohno, S. Suzuki, T. Nomura, C. Nishioka, T. Kashiwagi, T. Hirayama, M. Akiyama, R. Taguchi, H. Shimizu, S. Itohara, and A. Kihara Impaired epidermal permeability barrier in mice lacking ELOVL1, the gene responsible for very-long-chain fatty acid production Mol. Cell. Biol. 33 2013 2787 2796
41. A. McMahon, I.A. Butovich, N.L. Mata, M. Klein, R. Ritter III, J. Richardson, D.G. Birch, A.O. Edwards, and W. Kedzierski Retinal pathology and skin barrier defect in mice carrying a Stargardt disease-3 mutation in elongase of very long chain fatty acids-4 Mol. Vis. 13 2007 258 272 (Pubitemid 46323316)
42. D.J. Cameron, Z. Tong, Z. Yang, J. Kaminoh, S. Kamiyah, H. Chen, J. Zeng, Y. Chen, L. Luo, and K. Zhang Essential role of Elovl4 in very long chain fatty acid synthesis, skin permeability barrier function, and neonatal survival Int. J. Biol. Sci. 3 2007 111 119 (Pubitemid 46238637)
43. A. McMahon, I.A. Butovich, and W. Kedzierski Epidermal expression of an Elovl4 transgene rescues neonatal lethality of homozygous Stargardt disease-3 mice J. Lipid Res. 52 2011 1128 1138
44. K. Zhang, M. Kniazeva, M. Han, W. Li, Z. Yu, Z. Yang, Y. Li, M.L. Metzker, R. Allikmets, D.J. Zack, L.E. Kakuk, P.S. Lagali, P.W. Wong, I.M. MacDonald, P.A. Sieving, D.J. Figueroa, C.P. Austin, R.J. Gould, R. Ayyagari, and K. Petrukhin A 5-bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy Nat. Genet. 27 2001 89 93 (Pubitemid 32044525)
45. M.A. Aldahmesh, J.Y. Mohamed, H.S. Alkuraya, I.C. Verma, R.D. Puri, A.A. Alaiya, W.B. Rizzo, and F.S. Alkuraya Recessive mutations in ELOVL4 cause ichthyosis, intellectual disability, and spastic quadriplegia Am. J. Hum. Genet. 89 2011 745 750
46. Z. Jia, C.L. Moulson, Z. Pei, J.H. Miner, and P.A. Watkins Fatty acid transport protein 4 is the principal very long chain fatty acyl-CoA synthetase in skin fibroblasts J. Biol. Chem. 282 2007 20573 20583 (Pubitemid 47100017)
47. O. Inhoff, I. Hausser, S.W. Schneider, D. Khnykin, F.L. Jahnsen, J. Sartoris, S. Goerdt, and W.K. Peitsch Ichthyosis prematurity syndrome caused by a novel fatty acid transport protein 4 gene mutation in a German infant Arch. Dermatol. 147 2011 750 752
48. J. Klar, M. Schweiger, R. Zimmerman, R. Zechner, H. Li, H. Torma, A. Vahlquist, B. Bouadjar, N. Dahl, and J. Fischer Mutations in the fatty acid transport protein 4 gene cause the ichthyosis prematurity syndrome Am. J. Hum. Genet. 85 2009 248 253
49. T. Herrmann, F. van der Hoeven, H.J. Gröne, A.F. Stewart, L. Langbein, I. Kaiser, G. Liebisch, I. Gosch, F. Buchkremer, W. Drobnik, G. Schmitz, and W. Stremmel Mice with targeted disruption of the fatty acid transport protein 4 (Fatp 4, Slc27a4) gene show features of lethal restrictive dermopathy J. Cell Biol. 161 2003 1105 1115 (Pubitemid 36870172)
50. C.L. Moulson, D.R. Martin, J.J. Lugus, J.E. Schaffer, A.C. Lind, and J.H. Miner Cloning of wrinkle-free, a previously uncharacterized mouse mutation, reveals crucial roles for fatty acid transport protein 4 in skin and hair development Proc. Natl. Acad. Sci. U. S. A. 100 2003 5274 5279 (Pubitemid 36542695)
51. J. Rother, G. van Echten, G. Schwarzmann, and K. Sandhoff Biosynthesis of sphingolipids: dihydroceramide and not sphinganine is desaturated by cultured cells Biochem. Biophys. Res. Commun. 189 1992 14 20 (Pubitemid 23030001)
52. C. Michel, G. van Echten-Deckert, J. Rother, K. Sandhoff, E. Wang, and A.H. Merrill Jr. Characterization of ceramide synthesis. A dihydroceramide desaturase introduces the 4,5-trans-double bond of sphingosine at the level of dihydroceramide J. Biol. Chem. 272 1997 22432 22437 (Pubitemid 27386051)
53. T. Hornemann, Y. Wei, and A. von Eckardstein Is the mammalian serine palmitoyltransferase a high-molecular-mass complex? Biochem. J. 405 2007 157 164 (Pubitemid 46999936)
54. K.K. Hong, H.R. Cho, W.C. Ju, Y. Cho, and N.I. Kim A study on altered expression of serine palmitoyltransferase and ceramidase in psoriatic skin lesion J. Korean Med. Sci. 22 2007 862 867
55. K. Nakajima, M. Terao, M. Takaishi, S. Kataoka, N. Goto-Inoue, M. Setou, K. Horie, F. Sakamoto, M. Ito, H. Azukizawa, S. Kitaba, H. Murota, S. Itami, I. Katayama, J. Takeda, and S. Sano Barrier abnormality due to ceramide deficiency leads to psoriasiform inflammation in a mouse model J. Invest. Dermatol. 2013 10.1038/jid.2013.199 (accepted article preview online April 30, 2013)
56. K. Mizukoshi, K. Matsumoto, R. Hirose, T. Fujita, A. Ishida-Yamamoto, and H. Iizuka Effects of serine palmitoyltransferase inhibitor ISP-I on the stratum corneum of intact mouse skin Biol. Pharm. Bull. 34 2011 1383 1389
57. P. Ternes, S. Franke, U. Zahringer, P. Sperling, and E. Heinz Identification and characterization of a sphingolipid delta 4-desaturase family J. Biol. Chem. 277 2002 25512 25518 (Pubitemid 34951866)
58. M.E. Stewart, and D.T. Downing A new 6-hydroxy-4-sphingenine-containing ceramide in human skin J. Lipid Res. 40 1999 1434 1439 (Pubitemid 29379983)
59. Y. Pewzner-Jung, S. Ben-Dor, and A.H. Futerman When do Lasses (longevity assurance genes) become CerS (ceramide synthases)?: insights into the regulation of ceramide synthesis J. Biol. Chem. 281 2006 25001 25005 (Pubitemid 44401887)
60. W.M. Holleran, Y. Takagi, and Y. Uchida Epidermal sphingolipids: metabolism, function, and roles in skin disorders FEBS Lett. 580 2006 5456 5466 (Pubitemid 44465907)
61. K.M. Eckl, R. Tidhar, H. Thiele, V. Oji, I. Hausser, S. Brodesser, M.L. Preil, A. Önal-Akan, F. Stock, D. Müller, K. Becker, R. Casper, G. Nürnberg, J. Altmüller, P. Nürnberg, H. Traupe, A.H. Futerman, and H.C. Hennies Impaired epidermal ceramide synthesis causes autosomal recessive congenital ichthyosis and reveals the importance of ceramide acyl chain length J. Invest. Dermatol. 133 2013 2202 2211
62. Y. Mizutani, H. Sun, Y. Ohno, T. Sassa, T. Wakashima, M. Obara, K. Yuyama, A. Kihara, and Y. Igarashi Cooperative synthesis of ultra long-chain fatty acid and ceramide during keratinocyte differentiation PLoS One 8 2013 e67317
63. A. Hinder, C.E. Schmelzer, A.V. Rawlings, and R.H. Neubert Investigation of the molecular structure of the human stratum corneum ceramides [NP] and [EOS] by mass spectrometry Skin Pharmacol. Physiol. 24 2011 127 135
64. Y. Uchida, Y. Cho, S. Moradian, J. Kim, K. Nakajima, D. Crumrine, K. Park, M. Ujihara, M. Akiyama, H. Shimizu, W.M. Holleran, S. Sano, and P.M. Elias Neutral lipid storage leads to acylceramide deficiency, likely contributing to the pathogenesis of Dorfman-Chanarin syndrome J. Invest. Dermatol. 130 2010 2497 2499
65. F.P. Radner, I.E. Streith, G. Schoiswohl, M. Schweiger, M. Kumari, T.O. Eichmann, G. Rechberger, H.C. Koefeler, S. Eder, S. Schauer, H.C. Theussl, K. Preiss-Landl, A. Lass, R. Zimmermann, G. Hoefler, R. Zechner, and G. Haemmerle Growth retardation, impaired triacylglycerol catabolism, hepatic steatosis, and lethal skin barrier defect in mice lacking comparative gene identification-58 (CGI-58) J. Biol. Chem. 285 2010 7300 7311
66. K. Wakimoto, H. Chiba, H. Michibata, M. Seishima, S. Kawasaki, K. Okubo, H. Mitsui, H. Torii, and Y. Imai A novel diacylglycerol acyltransferase (DGAT2) is decreased in human psoriatic skin and increased in diabetic mice Biochem. Biophys. Res. Commun. 310 2003 296 302 (Pubitemid 37163663)
67. S.J. Stone, H.M. Myers, S.M. Watkins, B.E. Brown, K.R. Feingold, P.M. Elias, and R.V. Farese Jr. Lipopenia and skin barrier abnormalities in DGAT2-deficient mice J. Biol. Chem. 279 2004 11767 11776 (Pubitemid 38401682)
68. P.M. Elias, M.L. Williams, and K.R. Feingold Abnormal barrier function in the pathogenesis of ichthyosis: therapeutic implications for lipid metabolic disorders Clin. Dermatol. 30 2012 311 322
69. A.H. Futerman, and R.E. Pagano Determination of the intracellular sites and topology of glucosylceramide synthesis in rat liver Biochem. J. 280 1991 295 302
70. D. Jeckel, A. Karrenbauer, K.N. Burger, G. van Meer, and F. Wieland Glucosylceramide is synthesized at the cytosolic surface of various Golgi subfractions J. Cell Biol. 117 1992 259 267
71. K. Sandhoff, and T. Kolter Biosynthesis and degradation of mammalian glycosphingolipids Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 2003 847 861 (Pubitemid 36639708)
72. G. D'Angelo, E. Polishchuk, G. Di Tullio, M. Santoro, A. Di Campli, A. Godi, G. West, J. Bielawski, C.C. Chuang, A.C. van der Spoel, F.M. Platt, Y.A. Hannun, R. Polishchuk, P. Mattjus, and M.A. De Matteis Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide Nature 449 2007 62 67 (Pubitemid 47373773)
73. D. Halter, S. Neumann, S.M. van Dijk, J. Wolthoorn, A.M. de Maziere, O.V. Vieira, P. Mattjus, J. Klumperman, G. van Meer, and H. Sprong Pre- and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis J. Cell Biol. 179 2007 101 115 (Pubitemid 47606687)
74. H. Gallala, O. Macheleidt, T. Doering, V. Schreiner, and K. Sandhoff Nitric oxide regulates synthesis of gene products involved in keratinocyte differentiation and ceramide metabolism Eur. J. Cell Biol. 83 2004 667 679 (Pubitemid 40123831)
75. R. Jennemann, R. Sandhoff, L. Langbein, S. Kaden, U. Rothermel, H. Gallala, K. Sandhoff, H. Wiegandt, and H.-J. Gröne Integrity and barrier function of the epidermis critically depend on glucosylceramide synthesis J. Biol. Chem. 282 2007 3083 3094 (Pubitemid 47084363)
76. N. Amen, D. Mathow, M. Rabionet, R. Sandhoff, L. Langbein, N. Gretz, C. Jäckel, H.J. Gröne, and R. Jennemann Differentiation of epidermal keratinocytes is dependent on glucosylceramide: ceramide processing Hum. Mol. Genet. 2013 10.1093/hmg/ddt264 (accepted article preview online June 6, 2013)
77. R.K. Freinkel, and T.N. Traczyk Lipid composition and acid hydrolase content of lamellar granules of fetal rat epidermis J. Invest. Dermatol. 85 1985 295 298 (Pubitemid 15248011)
78. K.C. Madison, D.C. Swartzendruber, P.W. Wertz, and D.T. Downing Murine keratinocyte cultures grown at the air/medium interface synthesize stratum corneum lipids and "recycle" linoleate during differentiation J. Invest. Dermatol. 93 1989 10 17 (Pubitemid 19183305)
79. G.K. Menon, S. Grayson, and P.M. Elias Cytochemical and biochemical localization of lipase and sphingomyelinase activity in mammalian epidermis J. Invest. Dermatol. 86 1986 591 597 (Pubitemid 16052566)
80. G.K. Menon, R. Ghadially, M.L. Williams, and P.M. Elias Lamellar bodies as delivery systems of hydrolytic enzymes: implications for normal and abnormal desquamation Br. J. Dermatol. 126 1992 337 345
81. K.C. Madison, G.N. Sando, E.J. Howard, C.A. True, D. Gilbert, D.C. Swartzendruber, and P.W. Wertz Lamellar granule biogenesis: a role for ceramide glucosyltransferase, lysosomal enzyme transport, and the Golgi J. Investig. Dermatol. Symp. Proc. 3 1998 80 86 (Pubitemid 29135200)
82. T. Kolter, F. Winau, U.E. Schaible, M. Leippe, and K. Sandhoff Lipid-binding proteins in membrane digestion, antigen presentation, and antimicrobial defense J. Biol. Chem. 280 2005 41125 41128 (Pubitemid 41832164)
83. W.M. Holleran, E.I. Ginns, G.K. Menon, J.U. Grundmann, M. Fartasch, C.E. McKinney, P.M. Elias, and E. Sidransky Consequences of beta-glucocerebrosidase deficiency in epidermis. Ultrastructure and permeability barrier alterations in Gaucher disease J. Clin. Invest. 93 1994 1756 1764
84. G. Wilkening, T. Linke, and K. Sandhoff Lysosomal degradation on vesicular membrane surfaces. Enhanced glucosylceramide degradation by lysosomal anionic lipids and activators J. Biol. Chem. 273 1998 30271 30278 (Pubitemid 28545494)
85. E. Sidransky, D.M. Sherer, and E.I. Ginns Gaucher disease in the neonate: a distinct Gaucher phenotype is analogous to a mouse model created by targeted disruption of the glucocerebrosidase gene Pediatr. Res. 32 1992 494 498
86. M.E. Grace, P. Ashton-Prolla, G.M. Pastores, A. Soni, and R.J. Desnick Non-pseudogene-derived complex acid beta-glucosidase mutations causing mild type 1 and severe type 2 Gaucher disease J. Clin. Invest. 103 1999 817 823 (Pubitemid 29152627)
87. Y. Liu, K. Suzuki, J.D. Reed, A. Grinberg, H. Westphal, A. Hoffmann, T. Döring, K. Sandhoff, and R.L. Proia Mice with type 2 and 3 Gaucher disease point mutations generated by a single insertion mutagenesis procedure Proc. Natl. Acad. Sci. U. S. A. 95 1998 2503 2508 (Pubitemid 28145971)
88. N. Fujita, K. Suzuki, M.T. Vanier, B. Popko, N. Maeda, A. Klein, M. Henseler, K. Sandhoff, and H. Nakayasu Targeted disruption of the mouse sphingolipid activator protein gene: a complex phenotype, including severe leukodystrophy and wide-spread storage of multiple sphingolipids Hum. Mol. Genet. 5 1996 711 725 (Pubitemid 26171286)
89. Y. Zheng, H. Yin, W.E. Boeglin, P.M. Elias, D. Crumrine, D.R. Beier, and A.R. Brash Lipoxygenases mediate the effect of essential fatty acid in skin barrier formation: a proposed role in releasing omega-hydroxyceramide for construction of the corneocyte lipid envelope J. Biol. Chem. 286 2011 24046 24056
90. P. Krieg, S. Rosenberger, S. de Juanes, S. Latzko, J. Hou, A. Dick, U. Kloz, F. van der Hoeven, I. Hausser, I. Esposito, M. Rauh, and H. Schneider Aloxe3 knockout mice reveal a function of epidermal lipoxygenase-3 as hepoxilin synthase and its pivotal role in barrier formation J. Invest. Dermatol. 133 2013 172 180
91. N. Epp, G. Fürstenberger, K. Müller, S. de Juanes, M. Leitges, I. Hausser, F. Thieme, G. Liebisch, G. Schmitz, and P. Krieg 12R-lipoxygenase deficiency disrupts epidermal barrier function J. Cell Biol. 177 2007 173 182 (Pubitemid 46588410)
92. J.L. Moran, H. Qiu, A. Turbe-Doan, Y. Yun, W.E. Boeglin, A.R. Brash, and D.R. Beier A mouse mutation in the 12R-lipoxygenase, Alox12b, disrupts formation of the epidermal permeability barrier J. Invest. Dermatol. 127 2007 1893 1897 (Pubitemid 47075378)
93. M. Akiyama Harlequin ichthyosis and other autosomal recessive congenital ichthyoses: the underlying genetic defects and pathomechanisms J. Dermatol. Sci. 42 2006 83 89
94. K. Sandhoff My journey into the world of sphingolipids and sphingolipidoses Proc. Jpn. Acad. Ser. B 88 2012 554 582
95. T. Kolter, and K. Sandhoff Principles of lysosomal membrane digestion: stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids Annu. Rev. Cell Dev. Biol. 21 2005 81 103 (Pubitemid 41740628)
96. M. Abdul-Hammed, B. Breiden, M.A. Adebayo, J.O. Babalola, G. Schwarzmann, and K. Sandhoff Role of endosomal membrane lipids and NPC2 in cholesterol transfer and membrane fusion J. Lipid Res. 51 2010 1747 1760
97. F. Alessandrini, S. Pfister, E. Kremmer, J.-K. Gerber, J. Ring, and H. Behrendt Alterations of glucosylceramide-β-glucosidase levels in the skin of patients with psoriasis vulgaris J. Invest. Dermatol. 123 2004 1030 1036 (Pubitemid 39586822)
98. F. Alessandrini, S. Stachowitz, J. Ring, and H. Behrendt The level of prosaposin is decreased in the skin of patients with psoriasis vulgaris J. Invest. Dermatol. 116 2001 394 400 (Pubitemid 32202904)
99. T. Doering, H. Brade, and K. Sandhoff Sphingolipid metabolism during epidermal barrier development in mice J. Lipid Res. 43 2002 1727 1733 (Pubitemid 35168287)
100. K. Huitema, J. van den Dikkenberg, J.F. Brouwers, and J.C. Holthuis Identification of a family of animal sphingomyelin synthases EMBO J. 23 2004 33 44 (Pubitemid 38165745)
101. Y. Yoshida, K. Yoneda, M. Umeda, C. Ide, and K. Fujimoto Localization of sphingomyelin during the development of dorsal and tail epidermis of mice Br. J. Dermatol. 145 2001 758 770 (Pubitemid 33078346)
102. Y. Uchida, M. Hara, H. Nishio, E. Sidransky, S. Inoue, F. Otsuka, A. Suzuki, P.M. Elias, W.M. Holleran, and S. Hamanaka Epidermal sphingomyelins are precursors for selected stratum corneum ceramides J. Lipid Res. 41 2000 2071 2082 (Pubitemid 32039003)
103. J.M. Jensen, S. Schütze, M. Forl, M. Krönke, and E. Proksch Roles for tumor necrosis factor receptor p55 and sphingomyelinase in repairing the cutaneous permeability barrier J. Clin. Invest. 104 1999 1761 1770 (Pubitemid 30053193)
104. D. Kreder, O. Krut, S. Adam-Klages, K. Wiegmann, G. Scherer, T. Plitz, J.M. Jensen, E. Proksch, J. Steinmann, K. Pfeffer, and M. Krönke Impaired neutral sphingomyelinase activation and cutaneous barrier repair in FAN-deficient mice EMBO J. 18 1999 2472 2479 (Pubitemid 29213280)
105. M.J. Behne, J.W. Meyer, K.M. Hanson, N.P. Barry, S. Murata, D. Crumrine, R.W. Clegg, E. Gratton, W.M. Holleran, P.M. Elias, and T.M. Mauro NHE1 regulates the stratum corneum permeability barrier homeostasis. Microenvironment acidification assessed with fluorescence lifetime imaging J. Biol. Chem. 277 2002 47399 47406 (Pubitemid 36159255)
106. K.M. Hanson, M.J. Behne, N.P. Barry, T.M. Mauro, E. Gratton, and R.M. Clegg Two-photon fluorescence lifetime imaging of the skin stratum corneum pH gradient Biophys. J. 83 2002 1682 1690 (Pubitemid 34977738)
107. U. Rassner, K.R. Feingold, D.A. Crumrine, and P.M. Elias Coordinate assembly of lipids and enzyme proteins into epidermal lamellar bodies Tissue Cell 31 1999 489 498 (Pubitemid 29531291)
108. M. Schmuth, M.Q. Man, F. Weber, W. Gao, K.R. Feingold, P. Fritsch, P.M. Elias, and W.M. Holleran Permeability barrier disorder in Niemann-Pick disease: sphingomyelin-ceramide processing required for normal barrier homeostasis J. Invest. Dermatol. 115 2000 459 466
109. G. Vielhaber, S. Pfeiffer, L. Brade, B. Lindner, T. Goldmann, E. Vollmer, U. Hintze, K.P. Wittern, and R. Wepf Localization of ceramide and glucosylceramide in human epidermis by immunogold electron microscopy J. Invest. Dermatol. 117 2001 1126 1136 (Pubitemid 34205908)
110. S. Kusuda, C.Y. Cui, M. Takahashi, and T. Tezuka Localization of sphingomyelinase in lesional skin of atopic dermatitis patients J. Invest. Dermatol. 111 1998 733 738 (Pubitemid 28509310)
111. F. Sarmientos, G. Schwarzmann, and K. Sandhoff Specificity of human glucosylceramide beta-glucosidase towards synthetic glucosylsphingolipids inserted into liposomes. Kinetic studies in a detergent-free assay system Eur. J. Biochem. 160 1986 527 535 (Pubitemid 17044425)
112. S. Locatelli-Hoops, N. Remmel, R. Klingenstein, B. Breiden, M. Rossocha, M. Schoeniger, C. Koenigs, W. Saenger, and K. Sandhoff Saposin A mobilizes lipids from low cholesterol and high bis(monoacylglycerol)phosphate-containing membranes: patient variant saposin A lacks lipid extraction capacity J. Biol. Chem. 281 2006 32451 32460 (Pubitemid 46036800)
113. N. Remmel, S. Locatelli-Hoops, B. Breiden, G. Schwarzmann, and K. Sandhoff Saposin B mobilizes lipids from cholesterol-poor and bis(monoacylglycero)phosphate-rich membranes at acidic pH. Unglycosylated patient variant saposin B lacks lipid-extraction capacity FEBS J. 274 2007 3405 3420 (Pubitemid 47024974)
114. T. Linke, G. Wilkening, S. Lansmann, H. Moczall, O. Bartelsen, J. Weisgerber, and K. Sandhoff Stimulation of acid sphingomyelinase activity by lysosomal lipids and sphingolipid activator proteins Biol. Chem. 382 2001 283 290 (Pubitemid 32243936)
115. X. He, N. Okino, R. Dhami, A. Dagan, S. Gatt, H. Schulze, K. Sandhoff, and E.H. Schuchman Purification and characterization of recombinant, human acid ceramidase. Catalytic reactions and interactions with acid sphingomyelinase J. Biol. Chem. 278 2003 32978 32986 (Pubitemid 37055742)
116. V. Oninla, B. Breiden, J.O. Babalola, K. Sandhoff, (2013) in preparation.
117. J.A. Shayman, R. Kelly, J. Kollmeyer, Y. He, and A. Abe Group XV phospholipase A2, a lysosomal phospholipase A2 Prog. Lipid Res. 50 2011 1 13
118. B. Breiden, V.O. Oninla, K. Sandhoff, (2013) (in preparation).
119. G.K. Menon, S. Grayson, and P.M. Elias Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry J. Invest. Dermatol. 84 1985 508 512 (Pubitemid 15053207)
120. K.R. Feingold, and M. Denda Regulation of permeability barrier homeostasis Clin. Dermatol. 30 2012 263 268
121. C.L. Tu, D.A. Crumrine, M.Q. Man, W. Chang, H. Elalieh, M. You, P.M. Elias, and D.D. Bikle Ablation of the calcium-sensing receptor in keratinocytes impairs epidermal differentiation and barrier function J. Invest. Dermatol. 132 2012 2350 2359
122. K.R. Feingold, and Y.J. Jiang The mechanisms by which lipids coordinately regulate the formation of the protein and lipid domains of the stratum corneum: role of fatty acids, oxysterols, cholesterol sulfate and ceramides as signaling molecules Dermatoendocrinology 3 2011 113 118
123. M. Rivier, I. Castiel, I. Safonova, G. Ailhaud, and S. Michel Peroxisome proliferator-activated receptor-alpha enhances lipid metabolism in a skin equivalent model J. Invest. Dermatol. 114 2000 681 687 (Pubitemid 30227000)
124. Y.J. Jiang, B. Lu, P. Kim, G. Paragh, G. Schmitz, P.M. Elias, and K.R. Feingold PPAR and LXR activators regulate ABCA12 expression in human keratinocytes J. Invest. Dermatol. 128 2008 104 109 (Pubitemid 350249371)
125. M.-Q. Man, E.-H. Choi, M. Schmuth, D. Crumrine, Y. Uchida, P.M. Elias, W.M. Holleran, and K.R. Feingold Basis for improved permeability barrier homeostasis induced by PPAR and LXR activators: liposensors stimulate lipid synthesis, lamellar body secretion, and post-secretory lipid processing J. Invest. Dermatol. 126 2005 386 392 (Pubitemid 43323174)
126. M.R. Haussler, G.K. Whitfield, C.A. Haussler, J.C. Hsieh, P.D. Thompson, S.H. Selznick, C.E. Dominguez, and P.W. Jurutka The nuclear vitamin D receptor: biological and molecular regulatory properties revealed J. Bone Miner. 13 1998 325 349 (Pubitemid 28146215)
127. Y. Oda, C. Sihlbom, R.J. Chalkley, L. Huang, C. Rachez, C.P. Chang, A.L. Burlingame, L.P. Freedman, and D.D. Bikle Two distinct coactivators, DRIP/mediator and SRC/p160, are differentially involved in vitamin D receptor transactivation during keratinocyte differentiation Mol. Endocrinol. 17 2003 2329 2339 (Pubitemid 37352542)
128. Y. Oda, M.H. Ishikawa, N.P. Hawker, Q.C. Yun, and D.D. Bikle Differential role of two VDR coactivators, DRIP205 and SRC-3, in keratinocyte proliferation and differentiation J. Steroid Biochem. Mol. Biol. 103 2007 776 780 (Pubitemid 46401337)
129. Y. Oda, Y. Uchida, S. Moradian, D. Crumrine, P.M. Elias, and D.D. Bikle Vitamin D receptor and coactivators SRC2 and 3 regulate epidermis-specific sphingolipid production and permeability barrier formation J. Invest. Dermatol. 129 2009 1367 1378
130. T. Yoshizawa, Y. Handa, Y. Uematsu, S. Takeda, K. Sekine, Y. Yoshihara, T. Kawakami, K. Arioka, H. Sato, Y. Uchiyama, S. Masushige, A. Fukamizu, T. Matsumoto, and S. Kato Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning Nat. Genet. 16 1997 391 396 (Pubitemid 27323308)
131. M. Kypriotou, M. Huber, and D. Hohl The human epidermal differentiation complex: cornified envelope precursors, S100 proteins and the 'fused genes' family Exp. Dermatol. 21 2012 643 649
132. Z. Wang, J.S. Kirkwood, A.W. Taylor, J.F. Stevens, M. Leid, G. Ganguli-Indra, and A.K. Indra Transcription factor Ctip2 controls epidermal lipid metabolism and regulates expression of genes involved in sphingolipid biosynthesis during skin development J. Invest. Dermatol. 133 2013 668 676
133. O. Golonzhka, M. Leid, G. Indra, and A.K. Indra Expression of COUP-TF-interacting protein 2 (CTIP2) in mouse skin during development and in adulthood Gene Expr. Patterns 7 2007 754 760 (Pubitemid 47209496)
134. Z. Wang, L.J. Zhang, G. Guha, S. Li, K. Kyrylkova, C. Kioussi, M. Leid, G. Ganguli-Indra, and A.K. Indra Selective ablation of Ctip2/Bcl11b in epidermal keratinocytes triggers atopic dermatitis-like skin inflammatory responses in adult mice PLoS One 7 2012 e51262
135. O. Macheleidt, H.W. Kaiser, and K. Sandhoff Deficiency of epidermal protein-bound omega-hydroxyceramides in atopic dermatitis J. Invest. Dermatol. 119 2002 166 173 (Pubitemid 35304406)
136. M. Schüppel, U. Kürschner, U. Kleuser, M. Schäfer-Korting, and B. Kleuser Sphingosine 1-phosphate restrains insulin-mediated keratinocyte proliferation via inhibition of Akt through the S1P2 receptor subtype J. Invest. Dermatol. 128 2008 1747 1756 (Pubitemid 351847385)
137. A.C. Kendall, and A. Nicolaou Bioactive lipid mediators in skin inflammation and immunity Prog. Lipid Res. 52 2013 141 164
138. H. Hennings, D. Michael, C. Cheng, P. Steinert, K. Holbrook, and S.H. Yuspa Calcium regulation of growth and differentiation of mouse epidermal cells in culture Cell 19 1980 245 254 (Pubitemid 10154229)
139. M. Ponec, S. Gibbs, A. Weerheim, J. Kempenaar, A. Mulder, and A.M. Mommaas Epidermal growth factor and temperature regulate keratinocyte differentiation Arch. Dermatol. Res. 289 1997 317 326 (Pubitemid 27272011)
140. B. Breiden, H. Gallala, T. Doering, and K. Sandhoff Optimization of submerged keratinocyte cultures for the synthesis of barrier ceramides Eur. J. Cell Biol. 86 2007 657 673 (Pubitemid 350082201)
141. V. Krischel, D. Bruch-Gerharz, C. Suschek, K.D. Kröncke, T. Ruzicka, and V. Kolb-Bachofen Biphasic effect of exogenous nitric oxide on proliferation and differentiation in skin derived keratinocytes but not fibroblasts J. Invest. Dermatol. 111 1998 286 291 (Pubitemid 28354717)
142. D. Fehrenschild, U. Galli, B. Breiden, W. Bloch, P. Schettina, S. Brodesser, C. Michels, C. Günschmann, K. Sandhoff, C.M. Niessen, and C. Niemann TCF/Lef1-mediated control of lipid metabolism regulates skin barrier function J. Invest. Dermatol. 132 2012 337 345
143. C. Leyvraz, R.P. Charles, I. Rubera, M. Guitard, S. Rotman, B. Breiden, K. Sandhoff, and E. Hummler The epidermal barrier function is dependent on the serine protease CAP1/Prss8 J. Cell Biol. 170 2005 487 496 (Pubitemid 41126947)
144. S. Frateschi, E. Camerer, G. Crisante, S. Rieser, M. Membrez, R.-P. Charles, F. Beermann, J.-C. Stehle, B. Breiden, K. Sandhoff, S. Rotman, M. Haftek, A. Wilson, S. Ryser, M. Steinhoff, S.R. Coughlin, and E. Hummler PAR2 absence completely rescues inflammation and ichthyosis caused by altered CAP1/Prss8 expression in mouse skin Nat. Commun. 2 2011 161
145. C.K. Derian, A.J. Eckardt, and P. Andrade-Gordon Differential regulation of human keratinocyte growth and differentiation by a novel family of protease-activated receptors Cell Growth Differ. 8 1997 743 749 (Pubitemid 27287805)
146. J.P. Hachem, M.Q. Man, D. Crumrine, Y. Uchida, B.E. Brown, V. Rogiers, D. Roseeuw, K.R. Feingold, and P.M. Elias 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 2005 510 520
147. J.P. Hachem, E. Houben, D. Crumrine, M.Q. Man, N. Schurer, T. Roelandt, E.H. Choi, Y. Uchida, B.E. Brown, K.R. Feingold, and P.M. Elias Serine protease signaling of epidermal permeability barrier homeostasis J. Invest. Dermatol. 126 2006 2074 2086
148. R. Gareus, M. Huth, B. Breiden, A. Nenci, N. Rosch, I. Haase, W. Bloch, K. Sandhoff, and M. Pasparakis Normal epidermal differentiation but impaired skin-barrier formation upon keratinocyte-restricted IKK1 ablation Nat. Cell Biol. 9 2007 461 469 (Pubitemid 46511080)
149. R.P. Charles, M. Guitard, C. Leyvraz, B. Breiden, M. Haftek, Z. Haftek-Terreau, J.C. Stehle, K. Sandhoff, and E. Hummler Postnatal requirement of the epithelial sodium channel for maintenance of epidermal barrier function J. Biol. Chem. 283 2008 2622 2630
150. M. Schäfer, H. Farwanah, A.-H. Willrodt, A.J. Huebner, K. Sandhoff, D. Roop, D. Hohl, W. Bloch, and S. Werner Nrf2 links epidermal barrier function with antioxidant defense EMBO Mol. Med. 4 2012 364 379
151. M. Schäfer, A.-H. Willrodt, S. Kurinna, H.-D. Beer, H. Farwanah, A. Geusau, F. Gruber, O. Sorg, A.J. Huebner, D. Roop, K. Sandhoff, J.-H. Saurat, E. Tschachler, M.R. Schneider, L. Langbein, W. Bloch, and S. Werner Activation of Nrf2 in keratinocytes causes chloracne (MADISH)-like skin disease in mice EMBO Mol. Med. 2013 (in revision)