Impaired epidermal ceramide synthesis causes autosomal recessive congenital ichthyosis and reveals the importance of ceramide acyl chain length

Journal of Investigative Dermatology

Volumn 133, Issue 9, 2013, Pages 2202-2211

  Eckl, Katja Martina ^a,b   Tidhar, Rotem ^c   Thiele, Holger ^a   Oji, Vinzenz ^d   Hausser, Ingrid ^e   Brodesser, Susanne ^f   Preil, Marie Luise ^g   Önal Akan, Aysel ^a   Stock, Friedrich ^h   Müller, Dietmar ^h   Becker, Kerstin ^a   Casper, Ramona ^a   Nürnberg, Gudrun ^a   Altmüller, Janine ^a   Nürnberg, Peter ^a,f   Traupe, Heiko ^d   Futerman, Anthony H ^c   Hennies, Hans C ^a,b,f  

^a UNIVERSITY OF COLOGNE   (Germany)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^e UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^f UNIVERSITY OF COLOGNE   (Germany)

^g Practice for Dermatology Dres Krnjaic   (Germany)

^h UNIVERSITY HOSPITAL LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PYROXYLIN; SYNTHETASE;

ACYLATION; ANIMAL MODEL; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BIRTH; CHEMICAL STRUCTURE; CHROMOSOME; CLINICAL ARTICLE; CONSANGUINITY; ENZYME ACTIVITY; EPIDERMIS; ERYTHRODERMA; FEMALE; GENE EXPRESSION; GERMANY; HETEROZYGOTE; HUMAN; ICHTHYOSIS; KERATINOCYTE; LAMELLAR ICHTHYOSIS; LICHENOID ERUPTION; LIPID METABOLISM; LIPOGENESIS; MALASSEZIA DERMATITIS; MISSENSE MUTATION; MOUSE; NONHUMAN; PEDIGREE; PHENOTYPE; PRIORITY JOURNAL; TESTIS; UPREGULATION;

EID: 84884417429     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2013.153     Document Type: Article

References (55)

1. Abecasis GR, Cherny SS, Cookson WO et al. (2001) GRR: Graphical representation of relationship errors. Bioinformatics 17:742-3
2. Abecasis GR, Cherny SS, Cookson WO et al. (2002) Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet 30:97-101
3. Adzhubei IA, Schmidt S, Peshkin L et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248-9
4. Akiyama M, Sugiyama-Nakagiri Y, Sakai K et al. (2005) Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J Clin Invest 115:1777-84
5. Aldahmesh MA, Mohamed JY, Alkuraya HS et al. (2011) Recessive mutations in ELOVL4 cause ichthyosis, intellectual disability, and spastic quadriplegia. Am J Hum Genet 89:745-50
6. Allen-Hoffmann BL, Rheinwald JG (1984) Polycyclic aromatic hydrocarbon mutagenesis of human epidermal keratinocytes in culture. Proc Natl Acad Sci USA 81:7802-6
7. Ashkenazy H, Erez E, Martz E et al. (2010) ConSurf 2010: Calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38:W529-33
8. Behne M, Uchida Y, Seki T et al. (2000) Omega-hydroxyceramides are required for corneocyte lipid envelope (CLE) formation and normal epidermal permeability barrier function. J Invest Dermatol 114:185-92
9. Bouwstra JA, Ponec M (2006) The skin barrier in healthy and diseased state. Biochim Biophys Acta 1758:2080-95
10. Doering T, Proia RL, Sandhoff K (1999) Accumulation of protein-bound epidermal glucosylceramides in beta-glucocerebrosidase deficient type 2 Gaucher mice. FEBS Lett 447:167-70
11. Eckl KM, Alef T, Torres S et al. (2011) Full-Thickness human skin models for congenital ichthyosis and related keratinization disorders. J Invest Dermatol 131:1938-42
12. Elias PM (1987) Plastic wrap revisited. The stratum corneum two-compartment model and its clinical implications. Arch Dermatol 123:1405-6
13. Elias PM, Williams ML, Feingold KR (2012) Abnormal barrier function in the pathogenesis of ichthyosis: Therapeutic implications for lipid metabolic disorders. Clin Dermatol 30:311-22
14. Elias PM, Williams ML, Holleran WM et al. (2008) Pathogenesis of permeability barrier abnormalities in the ichthyoses: Inherited disorders of lipid metabolism. J Lipid Res 49:697-714
15. Gudbjartsson DF, Thorvaldsson T, Kong A et al. (2005) Allegro version 2. Nat Genet 37:1015-6
16. Hamanaka S, Hara M, Nishio H et al. (2002) Human epidermal glucosylceramides are major precursors of stratum corneum ceramides. J Invest Dermatol 119:416-23
17. Holleran WM, Ginns EI, Menon GK et al. (1994) Consequences of betaglucocerebrosidase deficiency in epidermis. Ultrastructure and permeability barrier alterations in Gaucher disease. J Clin Invest 93:1756-64
18. Iwai I, Han H, Hollander LD et al. (2012) The human skin barrier is organized as stacked bilayers of fully extended ceramides with cholesterol molecules associated with the ceramide sphingoid moiety. J Invest Dermatol 132:2215-25
19. Janušová B, Zbytovska J, Lorenc P et al. (2011) Effect of ceramide acyl chain length on skin permeability and thermotropic phase behavior of model stratum corneum lipid membranes. Biochim Biophys Acta 1811:129-37
20. Jennemann R, Rabionet M, Gorgas K et al. (2012) Loss of ceramide synthase 3 causes lethal skin barrier disruption. Hum Mol Genet 21:586-608
21. Jia Z, Moulson CL, Pei Z et al. (2007) Fatty acid transport protein 4 is the principal very long chain fatty acyl-CoA synthetase in skin fibroblasts. J Biol Chem 282:20573-83
22. Kageyama-Yahara N, Riezman H (2006) Transmembrane topology of ceramide synthase in yeast. Biochem J 398:585-93
23. Klar J, Schweiger M, Zimmerman R et al. (2009) Mutations in the fatty acid transport protein 4 gene cause the ichthyosis prematurity syndrome. Am J Hum Genet 85:248-53
24. Laviad EL, Albee L, Pankova-Kholmyansky I et al. (2008) Characterization of ceramide synthase 2: Tissue distribution, substrate specificity, and inhibition by sphingosine 1-phosphate. J Biol Chem 283:5677-84
25. Laviad EL, Kelly S, Merrill AH Jr. et al. (2012) Modulation of ceramide synthase activity via dimerization. J Biol Chem 287:21025-33
26. Lazo ND, Meine JG, Downing DT (1995) Lipids are covalently attached to rigid corneocyte protein envelopes existing predominantly as beta-sheets: A solid-state nuclear magnetic resonance study. J Invest Dermatol 105:296-300
27. Levy M, Futerman AH (2010) Mammalian ceramide synthases. IUBMB Life 62:347-56
28. Lopez O, Cocera M, Parra JL et al. (1999) Influence of ceramides in the solubilization of stratum corneum lipid liposomes by C(12)-betaine/ sodium dodecyl sulfate mixtures. Int J Pharm 187:231-41
29. Marekov LN, Steinert PM (1998) Ceramides are bound to structural proteins of the human foreskin epidermal cornified cell envelope. J Biol Chem 273:17763-70
30. Masukawa Y, Narita H, Shimizu E et al. (2008) Characterization of overall ceramide species in human stratum corneum. J Lipid Res 49:1466-76
31. Mesika A, Ben-Dor S, Laviad EL et al. (2007) A new functional motif in Hox domain-containing ceramide synthases: Identification of a novel region flanking the Hox and TLC domains essential for activity. J Biol Chem 282:27366-73
32. Mizutani Y, Kihara A, Chiba H et al. (2008) 2-Hydroxy-ceramide synthesis by ceramide synthase family: Enzymatic basis for the preference of FA chain length. J Lipid Res 49:2356-64
33. Mizutani Y, Kihara A, Igarashi Y (2006) LASS3 (longevity assurance homologue 3) is a mainly testis-specific (dihydro)ceramide synthase with relatively broad substrate specificity. Biochem J 398:531-8
34. Montero-Moran G, Caviglia JM, McMahon D et al. (2010) CGI-58/ABHD5 is a coenzyme A-dependent lysophosphatidic acid acyltransferase. J Lipid Res 51:709-19
35. Mullen TD, Hannun YA, Obeid LM (2012) Ceramide synthases at the centre of sphingolipid metabolism and biology. Biochem J 441:789-802
36. Nemes Z, Marekov LN, Fesus L et al. (1999) A novel function for transglutaminase 1: Attachment of long-chain omega-hydroxyceramides to involucrin by ester bond formation. Proc Natl Acad Sci USA 96:8402-7
37. Ng PC, Henikoff S (2001) Predicting deleterious amino acid substitutions. Genome Res 11:863-74
38. Oji V, Tadini G, Akiyama M et al. (2010) Revised nomenclature and classification of inherited ichthyoses: Results of the First Ichthyosis Consensus Conference in Soreze 2009. J Am Acad Dermatol 63:607-41
39. Oji V, Traupe H (2009) Ichthyosis: Clinical manifestations and practical treatment options. Am J Clin Dermatol 10:351-64
40. Pewzner-Jung Y, Ben-Dor S, Futerman AH (2006) When do Lasses (longevity assurance genes) become CerS (ceramide synthases)?: Insights into the regulation of ceramide synthesis. J Biol Chem 281:25001-5
41. Rabionet M, van der Spoel AC, Chuang CC et al. (2008) Male germ cells require polyenoic sphingolipids with complex glycosylation for completion of meiosis: A link to ceramide synthase-3. J Biol Chem283:13357-69
42. Radner FP, Streith IE, Schoiswohl G et al. (2010) Growth retardation, impaired triacylglycerol catabolism, hepatic steatosis, and lethal skin barrier defect in mice lacking comparative gene identification-58 (CGI-58). J Biol Chem 285:7300-11
43. Rheinwald JG, Green H (1974) Growth of cultured mammalian cells on secondary glucose sources. Cell 2:287-93
44. Rüschendorf F, Nürnberg P (2005) ALOHOMORA: A tool for linkage analysis using 10K SNP array data. Bioinformatics 21:2123-5
45. Schmuth M, Gruber R, Elias PM et al. (2007) Ichthyosis update: Towards a function-driven model of pathogenesis of the disorders of cornification and the role of corneocyte proteins in these disorders. Adv Dermatol 23:231-56
46. Schwamb J, Feldhaus V, Baumann M et al. (2012) B-cell receptor triggers drug sensitivity of primary CLL cells by controlling glucosylation of ceramides. Blood 120:3978-85
47. Shaner RL, Allegood JC, Park H et al. (2009) Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers. J Lipid Res 50:1692-707
48. Signorelli P, Hannun YA (2002) Analysis and quantitation of ceramide. Methods Enzymol 345:275-94
49. Spassieva S, Seo JG, Jiang JC et al. (2006) Necessary role for the Lag1p motif in (dihydro)ceramide synthase activity. J Biol Chem 281:33931-8
50. Teufel A, Maass T, Galle PR et al. (2009) The longevity assurance homologue of yeast lag1 (Lass) gene family. Int J Mol Med 23:135-40
51. Uchida Y, Cho Y, Moradian S et al. (2010) Neutral lipid storage leads to acylceramide deficiency, likely contributing to the pathogenesis of Dorfman-Chanarin syndrome. J Invest Dermatol 130:2497-9
52. Uchida Y, Holleran WM (2008) Omega-O-Acylceramide, alipid essential for mammalian survival. J Dermatol Sci 51:77-87
53. van den Ent F, Löwe J (2006) RF cloning: A restriction-free method for inserting target genes into plasmids. J Biochem Biophys Methods 67:67-74
54. van Smeden J, Hoppel L, van der Heijden R et al. (2011) LC/MS analysis of stratum corneum lipids: Ceramide profiling and discovery. J Lipid Res 52:1211-21
55. Zheng Y, Yin H, Boeglin WE et al. (2011) 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 286:24046-56