Differentiation of epidermal keratinocytes is dependent on glucosylceramide : Ceramide processing

Human Molecular Genetics

Volumn 22, Issue 20, 2013, Pages 4164-4179

  Amen, Nicole ^a   Mathow, Daniel ^a   Rabionet, Mariona ^a   Sandhoff, Roger ^a   Langbein, Lutz ^a   Gretz, Norbert ^b   Jäckel, Carsten ^c   Gröne, Hermann Josef ^a   Jennemann, Richard ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE GLUCOSYLTRANSFERASE; GLUCOSYLCERAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GAUCHER DISEASE; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GLYCOSYLATION; ICHTHYOSIS; KERATINOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROCESSING; SKIN PERMEABILITY; WATER PERMEABILITY; WOUND HEALING IMPAIRMENT;

ANIMALS; CELL DIFFERENTIATION; CERAMIDES; EPIDERMIS; GENE EXPRESSION PROFILING; GLUCOSYLCERAMIDES; GLUCOSYLTRANSFERASES; HUMANS; KERATINOCYTES; LIPIDS; MICE; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; PHENOTYPE; SIGNAL TRANSDUCTION; SKIN PHYSIOLOGICAL PHENOMENA;

EID: 84884717353     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt264     Document Type: Article

References (73)

1. Holleran, W.M., Takagi, Y. and Uchida, Y. (2006) Epidermal sphingolipids: metabolism, function, and roles in skin disorders. FEBS Lett., 580, 5456-5466.
2. Elias, P.M. (2012) Structure and function of the stratum corneum extracellular matrix. J. Invest. Dermatol., 132, 2131-2133.
3. Kolter, T. and Sandhoff, K. (1999) Sphingolipids-their metabolic pathways and the pathobiochemistry of neurodegenerative diseases. Angew. Chem. Int., 38, 1532-1568.
4. Sprong, H., Degroote, S., Nilsson, T., Kawakita, M., Ishida, N., van der Sluijs, P. and van Meer, G. (2003) Association of the Golgi UDP-galactose transporter with UDP-galactose:ceramide galactosyltransferase allows UDP-galactose import in the endoplasmic reticulum. Mol. Biol. Cell, 14, 3482-3493.
5. Madison, K.C.,Wertz, P.W., Strauss, J.S. and Downing, D.T. (1986) Lipid compositionof culturedmurinekeratinocytes. J. Invest.Dermatol.,87,253-259. 6. Sandhoff, R. (2009) Very long chain sphingolipids: tissue expression, function and synthesis. FEBS Lett., 584, 1907-1913.
6. Sandhoff, R. (2009) Very long chain sphingolipids: tissue expression, function and synthesis. FEBS Lett., 584, 1907-1913.
7. Doering, T., Proia, R.L. and Sandhoff, K. (1999) Accumulation of protein-bound epidermal glucosylceramides in beta-glucocerebrosidase deficient type 2 Gaucher mice. FEBS Lett., 447, 167-170.
8. Grayson, S., Johnson-Winegar, A.G., Wintroub, B.U., Isseroff, R.R., Epstein, E.H. Jr and Elias, P.M. (1985) Lamellar body-enriched fractions from neonatal mice: preparative techniques and partial characterization. J. Invest. Dermatol., 85, 289-294.
9. Vielhaber, G., Pfeiffer, S., Brade, L., Lindner, B., Goldmann, T., Vollmer, E., Hintze, U., Wittern, K.P. and Wepf, R. (2001) Localization of ceramide and glucosylceramide in human epidermis by immunogold electron microscopy. J. Invest. Dermatol., 117, 1126-1136.
10. Bouwstra, J.A., Honeywell-Nguyen, P.L., Gooris, G.S. and Ponec, M. (2003) Structure of the skin barrier and its modulation by vesicular formulations. Prog. Lipid Res., 42, 1-36.
11. Madison, K.C. (2003) Barrier function of the skin: 'la raison d'etre' of the epidermis. J. Invest. Dermatol., 121, 231-241.
12. Marekov, L.N. and Steinert, P.M. (1998) Ceramides are bound to structural proteins of the human foreskin epidermal cornified cell envelope. J. Biol. Chem., 273, 17763-17770.
13. Doering, T., Holleran, W.M., Potratz, A., Vielhaber, G., Elias, P.M., Suzuki, K. and Sandhoff, K. (1999) Sphingolipid activator proteins are required for epidermal permeability barrier formation. J. Biol. Chem., 274, 11038-11045.
14. Nemes, Z., Marekov, L.N., Fesus, L. and Steinert, P.M. (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, 8402-8407.
15. Jennemann, R., Rabionet, M., Gorgas, K., Epstein, S., Dalpke, A., Rothermel, U., Bayerle, A., van der Hoeven, F., Imgrund, S., Kirsch, J. et al. (2012) Loss of ceramide synthase 3 causes lethal skin barrier disruption. Hum. Mol. Genet., 21, 586-608.
16. Elias, P.M. (1983) Epidermal lipids, barrier function, and desquamation. J. Invest. Dermatol., 80 Suppl, 44s-49s.
17. Hamanaka, S., Hara, M., Nishio, H., Otsuka, F., Suzuki, A. and Uchida, Y. (2002)Humanepidermal glucosylceramides are major precursors of stratum corneum ceramides. J. Invest. Dermatol., 119, 416-423.
18. Jennemann, R., Sandhoff, R., Langbein, L., Kaden, S., Rothermel, U., Gallala, H., Sandhoff, K., Wiegandt, H. and Grone, H.J. (2007) Integrity and barrier function of the epidermis critically depend on glucosylceramide synthesis. J. Biol. Chem., 282, 3083-3094.
19. Fluhr, J.W. and Elias, P. (2002) Stratum corneumpH: formation and function of the Acid Mantle. Exog. Dermatol., 1, 163-175.
20. Candi, E., Schmidt, R. and Melino, G. (2005) The cornified envelope: a model of cell death in the skin. Nat. Rev. Mol. Cell Biol., 6, 328-340. 21. Simpson, C.L., Patel, D.M. and Green, K.J. (2011) Deconstructing the skin: cytoarchitectural determinants of epidermal morphogenesis. Nat. Rev. Mol. Cell Biol., 12, 565-580.
21. Simpson, C.L., Patel, D.M. and Green, K.J. (2011) Deconstructing the skin: cytoarchitectural determinants of epidermal morphogenesis. Nat. Rev. Mol. Cell Biol., 12, 565-580.
22. Jiang, Y.J., Uchida, Y., Lu, B., Kim, P., Mao, C., Akiyama, M., Elias, P.M., Holleran, W.M., Grunfeld, C. and Feingold, K.R. (2009) Ceramide stimulates ABCA12 expression via peroxisome proliferator-activated receptor {delta} in human keratinocytes. J. Biol. Chem., 284, 18942-18952.
23. Kannan-Thulasiraman, P., Seachrist, D.D., Mahabeleshwar, G.H., Jain, M.K. and Noy, N. (2010) Fatty acid-binding protein 5 and PPARbeta/delta are critical mediators of epidermal growth factor receptor-induced carcinoma cell growth. J. Biol. Chem., 285, 19106-19115.
24. Morgan, E., Kannan-Thulasiraman, P. and Noy, N. (2010) Involvement of fatty acid binding Protein 5 and PPARbeta/delta in prostate cancer cell growth. PPAR Res., doi:10.1155/2010/234629.
25. Han, J, Kioi, M., Chu, W.S., Kasperbauer, J.L., Strome, S.E. and Puri, R.K. (2009) Identification of potential therapeutic targets in human head & neck squamous cell carcinoma. Head Neck Oncol., 1, 27.
26. Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G. and Birchmeier, W. (2001) beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell, 105, 533-545.
27. Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., Noda, T., Kubo, A. and Tsukita, S. (2002) Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol., 156, 1099-1111.
28. Radner, F.P., Streith, I.E., Schoiswohl, G., Schweiger, M., Kumari, M., Eichmann, T.O., Rechberger, G., Koefeler, H.C., Eder, S., Schauer, S. et al. (2009) 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, 7300-7311.
29. Scharschmidt, T.C., Man, M.Q., Hatano, Y., Crumrine, D., Gunathilake, R., Sundberg, J.P., Silva, K.A., Mauro, T.M., Hupe, M., Cho, S. et al. (2009) Filaggrin deficiency confers a paracellular barrier abnormality that reduces inflammatory thresholds to irritants and haptens. J. Allergy Clin. Immunol., 124, 496-506, 506 e491-496.
30. Macheleidt, O., Kaiser, H.W. and Sandhoff, K. (2002) Deficiency of epidermal protein-bound omega-hydroxyceramides in atopic dermatitis. J. Invest. Dermatol., 119, 166-173.
31. Hong, K.K., Cho, H.R., Ju, W.C., Cho, Y. and Kim, N.I. (2007) A study on altered expression of serine palmitoyltransferase and ceramidase in psoriatic skin lesion. J. Korean Med. Sci., 22, 862-867.
32. Schuette, C.G., Doering, T., Kolter, T. and Sandhoff, K. (1999) The glycosphingolipidoses-from disease to basic principles of metabolism. Biol. Chem., 380, 759-766.
33. Zuo, Y., Zhuang, D.Z., Han, R., Isaac, G., Tobin, J.J., McKee, M., Welti, R., Brissette, J.L., Fitzgerald, M.L. and Freeman, M.W. (2008) ABCA12 maintains the epidermal lipid permeability barrier by facilitating formation of ceramide linoleic esters. J. Biol. Chem., 283, 36624-36635.
34. Ishida-Yamamoto, A., Kato, H., Kiyama, H., Armstrong, D.K., Munro, C.S., Eady, R.A., Nakamura, S., Kinouchi, M., Takahashi, H. and Iizuka, H. (2000) Mutant loricrin is not crosslinked into the cornified cell envelope but is translocated into the nucleus in loricrin keratoderma. J. Invest. Dermatol., 115, 1088-1094.
35. Palmer, C.N., Irvine, A.D., Terron-Kwiatkowski, A., Zhao, Y., Liao, H., Lee, S.P., Goudie, D.R., Sandilands, A., Campbell, L.E., Smith, F.J. et al. (2006) Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat. Genet., 38, 441-446.
36. Weidinger, S., Illig, T., Baurecht, H., Irvine, A.D., Rodriguez, E., Diaz-Lacava, A., Klopp, N., Wagenpfeil, S., Zhao, Y., Liao, H. et al. (2006) Loss-of-function variations within the filaggrin gene predispose for atopic dermatitis with allergic sensitizations. J. Allergy Clin. Immunol., 118, 214-219.
37. Hansmann, B., Ahrens, K., Wu, Z., Proksch, E., Meyer-Hoffert, U. and Schroder, J.M. (2012) Murine filaggrin-2 is involved in epithelial barrier function and down-regulated in metabolically induced skin barrier dysfunction. Exp. Dermatol., 21, 271-276.
38. Sandilands, A., Sutherland, C., Irvine, A.D. and McLean, W.H. (2009) Filaggrin in the frontline: role in skin barrier function and disease. J. Cell Sci., 122, 1285-1294.
39. Holleran, W.M., Takagi, Y., Imokawa, G., Jackson, S., Lee, J.M. and Elias, P.M. (1992) beta-Glucocerebrosidase activity in murine epidermis: characterization and localization in relation to differentiation. J. Lipid Res., 33, 1201-1209.
40. Schmuth, M., Man, M.Q., Weber, F., Gao, W., Feingold, K.R., Fritsch, P., Elias, P.M. and Holleran, W.M. (2000) Permeability barrier disorder in Niemann-Pick disease: sphingomyelin-ceramide processing required for normal barrier homeostasis. J. Invest. Dermatol., 115, 459-466.
41. Fluhr, J.W., Kao, J., Jain, M., Ahn, S.K., Feingold, K.R. and Elias, P.M. (2001) Generation of free fatty acids from phospholipids regulates stratum corneum acidification and integrity. J. Invest. Dermatol., 117, 44-51.
42. Ohman, H. and Vahlquist, A. (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.
43. Lin, T.K., Crumrine, D., Ackerman, L.D., Santiago, J.L., Roelandt, T., Uchida, Y., Hupe, M., Fabrias, G., Abad, J.L., Rice, R.H. et al. (2012) Cellular changes that accompany shedding of human corneocytes. J. Invest. Dermatol., 132, 2430-2439.
44. Chujor, C.S., Feingold, K.R., Elias, P.M. and Holleran, W.M. (1998) Glucosylceramide synthase activity in murine epidermis: quantitation, localization, regulation, and requirement for barrier homeostasis. J. Lipid Res., 39, 277-285.
45. Grubauer, G., Feingold, K.R. and Elias, P.M. (1987) Relationship of epidermal lipogenesis to cutaneous barrier function. J. Lipid Res., 28, 746- 752.
46. Geilen, C.C., Wieder, T. and Orfanos, C.E. (1997) Ceramide signalling: regulatory role in cell proliferation, differentiation and apoptosis in human epidermis. Arch. Dermatol. Res., 289, 559-566.
47. Schiffmann, S., Sandner, J., Birod, K., Wobst, I., Angioni, C., Ruckhaberle, E., Kaufmann, M., Ackermann, H., Lotsch, J., Schmidt, H. et al. (2009) Ceramide synthases and ceramide levels are increased in breast cancer tissue. Carcinogenesis, 30, 745-752.
48. Hartmann, D., Lucks, J., Fuchs, S., Schiffmann, S., Schreiber, Y., Ferreiros, N., Merkens, J., Marschalek, R., Geisslinger, G. and Grosch, S. (2012) Long chain ceramides and very long chain ceramides have opposite effects on human breast and colon cancer cell growth. Int. J. Biochem. Cell Biol., 44, 620-628.
49. Koybasi, S., Senkal, C.E., Sundararaj, K., Spassieva, S., Bielawski, J., Osta, W., Day, T.A., Jiang, J.C., Jazwinski, S.M., Hannun, Y.A. et al. (2004) Defects in cell growth regulation by C18:0-ceramide and longevity assurance gene 1 in human head and neck squamous cell carcinomas. J. Biol. Chem., 279, 44311-44319.
50. Eto, M., Bennouna, J., Hunter, O.C., Lotze, M.T. and Amoscato, A.A. (2006) Importance of C16 ceramide accumulation during apoptosis in prostate cancer cells. Int. J. Urol., 13, 148-156.
51. Eming, S.A., Krieg, T. and Davidson, J.M. (2007) Inflammation in wound repair: molecular and cellular mechanisms. J. Invest. Dermatol., 127, 514- 525.
52. Uchida, Y., Hamanaka, S., Matsuda, K., Mimura, K. and Otsuka, F. (1996) Effect of a chemically-synthesized acylglucosylceramide, epidermoside, on normal human keratinocyte differentiation. J. Dermatol. Sci., 12, 64-68.
53. Uchida, Y., Iwamori,M.and Nagai, Y. (1990) Activation of keratinization of keratinocytes from fetal rat skin with N-(O-linoleoyl) omega-hydroxy fatty acyl sphingosyl glucose (lipokeratinogenoside) as a marker of epidermis. Biochem. Biophys. Res. Commun., 170, 162-168.
54. Uchida, Y., Ogawa, T., Iwamori, M. and Nagai, Y. (1991) Enhancement of keratin synthesis induced by lipokeratinogenoside, N-(O-linoleoyl)-omega-hydroxy fatty acyl sphingosyl glucose, in association with alteration of the intracellular Ca(2+)-content and protein kinase in cultured keratinocytes (FRSK). J. Biochem., 109, 462-465.
55. Kypriotou, M., Huber, M. and Hohl, D. (2012) The human epidermal differentiation complex: cornified envelope precursors, S100 proteins and the 'fused genes' family. Exp. Dermatol., 21, 643-649.
56. Cork, M.J., Danby, S.G., Vasilopoulos, Y., Hadgraft, J., Lane, M.E., Moustafa, M., Guy, R.H., Macgowan, A.L., Tazi-Ahnini, R. and Ward, S.J. (2009) Epidermal barrier dysfunction in atopic dermatitis. J. Invest. Dermatol., 129, 1892-1908.
57. Bergboer, J.G., Tjabringa, G.S., Kamsteeg, M., van Vlijmen-Willems, I.M., Rodijk-Olthuis, D., Jansen, P.A., Thuret, J.Y., Narita, M., Ishida-Yamamoto, A., Zeeuwen, P.L. et al. (2011) Psoriasis risk genes of the late cornified envelope-3 group are distinctly expressed compared with genes of other LCE groups. Am. J. Pathol., 178, 1470-1477.
58. Iizuka, H., Takahashi, H., Honma, M. and Ishida-Yamamoto, A. (2004) Unique keratinization process in psoriasis: late differentiation markers are abolished because of the premature cell death. J. Dermatol., 31, 271-276.
59. Komatsu, N., Saijoh, K., Kuk, C., Liu, A.C., Khan, S., Shirasaki, F., Takehara, K. and Diamandis, E.P. (2007) Human tissue kallikrein expression in the stratum corneum and serum of atopic dermatitis patients. Exp. Dermatol., 16, 513-519.
60. Akiyama, M., Sugiyama-Nakagiri, Y., Sakai, K., McMillan, J.R., Goto, M., Arita, K., Tsuji-Abe, Y., Tabata, N., Matsuoka, K., Sasaki, R. et al. (2005) Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J. Clin. Invest., 115, 1777- 1784.
61. Jennemann, R., Sandhoff, R., Wang, S., Kiss, E., Gretz, N., Zuliani, C., Martin-Villalba, A., Jager, R., Schorle, H., Kenzelmann, M. et al. (2005) Cell-specific deletion of glucosylceramide synthase in brain leads to severe neural defects after birth. Proc. Natl Acad. Sci. USA, 102, 12459-12464.
62. Rodriguez, C.I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A.F. and Dymecki, S.M. (2000) High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet., 25, 139-140.
63. Mertens, A.E., Rygiel, T.P., Olivo, C., van der Kammen, R. and Collard, J.G. (2005) The Rac activator Tiam1 controls tight junction biogenesis in keratinocytes through binding to and activation of the Par polarity complex. J. Cell Biol., 170, 1029-1037.
64. Jennemann, R., Kaden, S., Sandhoff, R., Nordstrom, V., Wang, S., Volz, M., Robine, S., Amen, N., Rothermel, U., Wiegandt, H. et al. (2012) Glycosphingolipids are essential for intestinal endocytic function. J. Biol. Chem., 287, 32598-32616.
65. Imokawa, G., Abe, A., Jin, K., Higaki, Y., Kawashima, M. and Hidano, A. (1991) Decreased level of ceramides in stratum corneum of atopic dermatitis: an etiologic factor in atopic dry skin? J. Invest. Dermatol., 96, 523-526.
66. Takagi, Y., Kriehuber, E., Imokawa, G., Elias, P.M. and Holleran, W.M. (1999) Beta-glucocerebrosidase activity in mammalian stratum corneum. J. Lipid. Res., 40, 861-869.
67. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
68. el Marjou, F., Janssen, K.P., Chang, B.H., Li, M., Hindie, V., Chan, L., Louvard, D., Chambon, P., Metzger, D. and Robine, S. (2004) Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis, 39, 186-193.
69. Greenspan, P., Mayer, E.P. and Fowler, S.D. (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J. Cell Biol., 100, 965-973.
70. Diaz, L.A., Heaphy, M.R., Calvanico, N.J., Tomasi, T.B. and Jordon, R.E. (1977) Separation of epidermis from dermis with sodium thiocyanate. J. Invest. Dermatol., 68, 36-38.
71. Chomczynski, P. and Sacchi, N. (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat. Protoc., 1, 581-585.
72. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. and Speed, T.P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
73. Edgar, R.,Domrachev,M.and Lash, A.E. (2002)GeneExpressionOmnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res., 30, 207-210.