Producing human ceramide-NS by metabolic engineering using yeast Saccharomyces cerevisiae

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Murakami, Suguru ^a   Shimamoto, Toshi ^a   Nagano, Hideaki ^b   Tsuruno, Masahiro ^a   Okuhara, Hiroaki ^b   Hatanaka, Haruyo ^b   Tojo, Hiromasa ^c   Kodama, Yukiko ^b   Funato, Kouichi ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b SUNTORY LTD   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE DIHYDROCERAMIDASE, S CEREVISIAE; AMIDASE; ANTIFUNGAL AGENT; AUREOBASIDIN A; CERAMIDE; DEPSIPEPTIDE; DIHYDROCERAMIDE DESATURASE; ISC1 PROTEIN, S CEREVISIAE; MIXED FUNCTION OXIDASE; OXIDOREDUCTASE; PHOSPHOLIPASE C; SACCHAROMYCES CEREVISIAE PROTEIN; SCS7 PROTEIN, S CEREVISIAE; SPHINGOSINE; SUR2 PROTEIN, S CEREVISIAE;

AMINO ACID SEQUENCE; DEFICIENCY; DRUG EFFECTS; ENDOPLASMIC RETICULUM; FLUORESCENCE MICROSCOPY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; METABOLIC ENGINEERING; METABOLISM; MICROBIOLOGY; PROCEDURES; SACCHAROMYCES CEREVISIAE; TANDEM MASS SPECTROMETRY;

AMIDOHYDROLASES; AMINO ACID SEQUENCE; ANTIFUNGAL AGENTS; CERAMIDES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DEPSIPEPTIDES; ENDOPLASMIC RETICULUM; HUMANS; INDUSTRIAL MICROBIOLOGY; METABOLIC ENGINEERING; MICROSCOPY, FLUORESCENCE; MIXED FUNCTION OXYGENASES; OXIDOREDUCTASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPHINGOSINE; TANDEM MASS SPECTROMETRY; TYPE C PHOSPHOLIPASES;

EID: 84947810654     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep16319     Document Type: Article

References (51)

1. Bouwstra, J. A. and Ponec, M. The skin barrier in healthy and diseased state. Biochim Biophys Acta 1758, 2080-2095 (2006).
2. Holleran, W. M., Takagi, Y. and Uchida, Y. Epidermal sphingolipids: metabolism, function, and roles in skin disorders. FEBS Lett 580, 5456-5466 (2006).
3. Mizutani, Y., Mitsutake, S., Tsuji, K., Kihara, A. and Igarashi, Y. Ceramide biosynthesis in keratinocyte and its role in skin function. Biochimie 91, 784-790 (2009).
4. Nishifuji, K. and Yoon, J. S. The stratum corneum: the rampart of the mammalian body. Vet Dermatol 24, 60-72. e15-66 (2013).
5. Imokawa, G. et al. Decreased level of ceramides in stratum corneum of atopic dermatitis: an etiologic factor in atopic dry skin? J Invest Dermatol 96, 523-526 (1991).
6. Di Nardo, A., Wertz, P., Giannetti, A. and Seidenari, S. Ceramide and cholesterol composition of the skin of patients with atopic dermatitis. Acta Derm Venereol 78, 27-30 (1998).
7. Elias, P. M. and Wakefield, J. S. Mechanisms of abnormal lamellar body secretion and the dysfunctional skin barrier in patients with atopic dermatitis. J Allergy Clin Immunol 134, 781-791. e781 (2014).
8. Kim, D. S. et al. Delayed ERK activation by ceramide reduces melanin synthesis in human melanocytes. Cell Signal 14, 779-785 (2002).
9. De Paepe, K., Roseeuw, D. and Rogiers, V. Repair of acetone- and sodium lauryl sulphate-damaged human skin barrier function using topically applied emulsions containing barrier lipids. J Eur Acad Dermatol Venereol 16, 587-594 (2002).
10. Huang, H. C. and Chang, T. M. Ceramide 1 and ceramide 3 act synergistically on skin hydration and the transepidermal water loss of sodium lauryl sulfate-irritated skin. Int J Dermatol 47, 812-819 (2008).
11. Meckfessel, M. H. and Brandt, S. The structure, function, and importance of ceramides in skin and their use as therapeutic agents in skin-care products. J Am Acad Dermatol 71, 177-184 (2014).
12. Takagi, S. et al. Alteration of the 4-sphingenine scaffolds of ceramides in keratinocyte-specific Arnt-deficient mice affects skin barrier function. J Clin Invest 112, 1372-1382 (2003).
13. Janssens, M. et al. Increase in short-chain ceramides correlates with an altered lipid organization and decreased barrier function in atopic eczema patients. J Lipid Res 53, 2755-2766 (2012).
14. Li, W. et al. 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, 120-128 (2007).
15. Kwun, K. H., Lee, J. H., Rho, K. H. and Yun, H. S. Production of ceramide with Saccharomyces cerevisiae. Appl Biochem Biotechnol 133, 203-210 (2006).
16. Kim, S. K., Noh, Y. H., Koo, J. R. and Yun, H. S. Effect of expression of genes in the sphingolipid synthesis pathway on the biosynthesis of ceramide in Saccharomyces cerevisiae. J Microbiol Biotechnol 20, 356-362 (2010).
17. Takakuwa, N., Saito, K., Ohnishi, M. and Oda, Y. Determination of glucosylceramide contents in crop tissues and by-products from their processing. Bioresour Technol 96, 1089-1092 (2005).
18. Wang, L., Wang, T. and Fehr, W. R. HPLC quantification of sphingolipids in soybeans with modified palmitate content. J Agric Food Chem 54, 7422-7428 (2006).
19. Konig, S. et al. Arabidopsis mutants of sphingolipid fatty acid alpha-hydroxylases accumulate ceramides and salicylates. New Phytol 196, 1086-1097 (2012).
20. Ternes, P., Franke, S., Zahringer, U., Sperling, P. and Heinz, E. Identification and characterization of a sphingolipid delta 4-desaturase family. J Biol Chem 277, 25512-25518 (2002).
21. Rao, R. P. and Acharya, J. K. Sphingolipids and membrane biology as determined from genetic models. Prostaglandins Other Lipid Mediat 85, 1-16 (2008).
22. Haak, D., Gable, K., Beeler, T. and Dunn, T. Hydroxylation of Saccharomyces cerevisiae ceramides requires Sur2p and Scs7p. J Biol Chem 272, 29704-29710 (1997).
23. Dickson, R. C. Thematic review series: sphingolipids. New insights into sphingolipid metabolism and function in budding yeast. J Lipid Res 49, 909-921 (2008).
24. Funato, K. and Riezman, H. Vesicular and nonvesicular transport of ceramide from ER to the Golgi apparatus in yeast. J Cell Biol 155, 949-959 (2001).
25. Nagiec, M. M. et al. Sphingolipid synthesis as a target for antifungal drugs. Complementation of the inositol phosphorylceramide synthase defect in a mutant strain of Saccharomyces cerevisiae by the AUR1 gene. J Biol Chem 272, 9809-9817 (1997).
26. Mao, C., Xu, R., Bielawska, A., Szulc, Z. M. and Obeid, L. M. Cloning and characterization of a Saccharomyces cerevisiae alkaline ceramidase with specificity for dihydroceramide. J Biol Chem 275, 31369-31378 (2000).
27. Sawai, H. et al. Identification of ISC1 (YER019w) as inositol phosphosphingolipid phospholipase C in Saccharomyces cerevisiae. J Biol Chem 275, 39793-39798 (2000).
28. Tani, M. and Kuge, O. Hydroxylation state of fatty acid and long-chain base moieties of sphingolipid determine the sensitivity to growth inhibition due to AUR1 repression in Saccharomyces cerevisiae. Biochem Biophys Res Commun 417, 673-678 (2012).
29. Epstein, S., Castillon, G. A., Qin, Y. and Riezman, H. An essential function of sphingolipids in yeast cell division. Mol Microbiol 84, 1018-1032 (2012).
30. Kajiwara, K. et al. Perturbation of sphingolipid metabolism induces endoplasmic reticulum stress-mediated mitochondrial apoptosis in budding yeast. Mol Microbiol 86, 1246-1261 (2012).
31. Cerantola, V. et al. Aureobasidin A arrests growth of yeast cells through both ceramide intoxication and deprivation of essential inositolphosphorylceramides. Mol Microbiol 71, 1523-1537 (2009).
32. Guan, X. L. et al. Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol Biol Cell 20, 2083-2095 (2009).
33. Ikeda, A. et al. Sphingolipids regulate telomere clustering by affecting transcriptional levels of genes involved in telomere homeostasis. J Cell Sci 128, 2454-2467 (2015).
34. Mizutani, Y., Kihara, A. and Igarashi, Y. Identification of the human sphingolipid C4-hydroxylase, hDES2, and its up-regulation during keratinocyte differentiation. FEBS Lett 563, 93-97 (2004).
35. Idkowiak-Baldys, J. et al. Dihydroceramide desaturase activity is modulated by oxidative stress. Biochem J 427, 265-274 (2010).
36. Cadena, D. L., Kurten, R. C. and Gill, G. N. The product of the MLD gene is a member of the membrane fatty acid desaturase family: overexpression of MLD inhibits EGF receptor biosynthesis. Biochemistry 36, 6960-6967 (1997).
37. Matsuyama, A. et al. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 24, 841-847 (2006).
38. Natter, K. et al. The spatial organization of lipid synthesis in the yeast Saccharomyces cerevisiae derived from large scale green fluorescent protein tagging and high resolution microscopy. Mol Cell Proteomics 4, 662-672 (2005).
39. Jackson, M. R., Nilsson, T. and Peterson, P. A. Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. Embo j 9, 3153-3162 (1990).
40. Cosson, P. and Letourneur, F. Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263, 1629-1631 (1994).
41. Letourneur, F. et al. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79, 1199-1207 (1994).
42. Huang, X., Withers, B. R. and Dickson, R. C. Sphingolipids and lifespan regulation. Biochim Biophys Acta 1841, 657-664 (2014).
43. Huang, X., Liu, J. and Dickson, R. C. Down-regulating sphingolipid synthesis increases yeast lifespan. PLoS Genet 8, e1002493 (2012).
44. Vionnet, C., Roubaty, C., Ejsing, C. S., Knudsen, J. and Conzelmann, A. Yeast cells lacking all known ceramide synthases continue to make complex sphingolipids and to incorporate ceramides into glycosylphosphatidylinositol (GPI) anchors. J Biol Chem 286, 6769-6779 (2011).
45. Kajiwara, K. et al. Yeast ARV1 is required for efficient delivery of an early GPI intermediate to the first mannosyltransferase during GPI assembly and controls lipid flow from the endoplasmic reticulum. Mol Biol Cell 19, 2069-2082 (2008).
46. Kajiwara, K. et al. Osh proteins regulate COPII-mediated vesicular transport of ceramide from the endoplasmic reticulum in budding yeast. J Cell Sci 127, 376-387 (2014).
47. Triola, G. et al. Specificity of the dihydroceramide desaturase inhibitor N-[(1R,2S)-2-hydroxy-1-hydroxymethyl-2-(2-tridecyl-1- cyclopropenyl)ethyl]octanami de (GT11) in primary cultured cerebellar neurons. Mol Pharmacol 66, 1671-1678 (2004).
48. Sperling, P., Zahringer, U. and Heinz, E. A sphingolipid desaturase from higher plants. Identification of a new cytochrome b5 fusion protein. J Biol Chem 273, 28590-28596 (1998).
49. Mizutani, Y., Kihara, A., Chiba, H., Tojo, H. and Igarashi, Y. 2-Hydroxy-ceramide synthesis by ceramide synthase family: enzymatic basis for the preference of FA chain length. J Lipid Res 49, 2356-2364 (2008).
50. Funato, K., Lombardi, R., Vallee, B. and Riezman, H. Lcb4p is a key regulator of ceramide synthesis from exogenous long chain sphingoid base in Saccharomyces cerevisiae. J Biol Chem 278, 7325-7334 (2003).
51. Motta, S. et al. Ceramide composition of the psoriatic scale. Biochim Biophys Acta 1182, 147-151 (1993).