Lipidome of narrow-band ultraviolet B irradiated keratinocytes shows apoptotic hallmarks

Experimental Dermatology

Volumn 19, Issue 8, 2010, Pages

  Reich, Adam ^a   Schwudke, Dominik ^b,d   Meurer, Michael ^c   Lehmann, Bodo ^c   Shevchenko, Andrej ^b  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Apoptosis; Keratinocytes; Mass spectrometry; Shotgun lipidomics; UV light

Indexed keywords

ACETIC ACID ETHYL ESTER; ALCOHOL; CERAMIDE; CHLOROFORM; HEXANE; LIPIDOME; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; SHORT CHAIN FATTY ACID; SILICON DIOXIDE; TRIACYLGLYCEROL; TRIETHYLAMINE; WATER;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL IMMORTALIZATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; KERATINOCYTE; LIPIDOMICS; TIME; ULTRAVIOLET B RADIATION;

APOPTOSIS; CELLS, CULTURED; CERAMIDES; DOSE-RESPONSE RELATIONSHIP, RADIATION; HUMANS; KERATINOCYTES; LIPID METABOLISM; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; TIME FACTORS; TRIGLYCERIDES; ULTRAVIOLET RAYS;

EID: 77954859199     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2009.01000.x     Document Type: Article

References (52)

1. Bissett D L, Hannon D P, Orr T V. Wavelength dependence of histological, physical, and visible changes in chronically UV-irradiated hairless mouse skin. Photochem Photobiol 1989, 50:763-769.
2. Van Weelden H, Young E, van der Leun J C. Therapy of psoriasis: comparison of photochemotherapy and several variants of phototherapy. Br J Dermatol 1980, 103:1-9.
3. Parrish J A, Jaenicke K F. Action spectrum for phototherapy of psoriasis. J Invest Dermatol 1981, 76:359-362.
4. Bandow G D, Koo J Y M. Narrow-band ultraviolet B radiation: a review of the current literature. Int J Dermatol 2004, 43:555-561.
5. Kunisada M, Kumimoto H, Ishizaki K, Sakumi K, Nakabeppu Y, Nishigori C. Narrow-band UVB induces more carcinogenic skin tumors than broad-band UVB through the formation of cyclobutane pyrimidine dimer. J Invest Dermatol 2007, 127:2865-2871.
6. Hearn R M, Kerr A C, Rahim K F, Ferguson J, Dawe R S. Incidence of skin cancers in 3867 patients treated with narrow-band ultraviolet B phototherapy. Br J Dermatol 2008, 159:931-935.
7. Macve J C, Norval M. The effects of UV waveband and cis-urocanic acid on tumour outgrowth in mice. Photochem Photobiol Sci 2002, 1:1006-1011.
8. Yule S, Dawe R S, Cameron H, Ferguson J, Ibbotson S H. Does narrow-band ultraviolet B phototherapy work in atopic dermatitis through a local or a systemic effect? Photodermatol Photoimmunol Photomed 2005, 21:333-335.
9. Ozawa M, Ferenczi K, Kikuchi T. 312-nanometer ultraviolet B light (narrow-band UVB) induces apoptosis of T cells within psoriatic lesions. J Exp Med 1999, 189:711-718.
10. Piskin G, Sylva-Steenland R M R, Bos J D, Teunissen M B M. T cells in psoriatic lesional skin that survive conventional therapy with NB-UVB radiation display reduced IFN-γ expression. Arch Dermatol Res 2004, 295:509-516.
11. Sigmundsdottir H, Johnston A, Gudjonsson J E, Valdimarsson H. Narrowband-UVB irradiation decreases the production of pro-inflammatory cytokines by stimulated T cells. Arch Dermatol Res 2005, 297:39-42.
12. Lehmann B, Knuschke P, Meurer M. UVB-induced conversion of 7-dehydrocholesterol to 1α,25-dihydroxyvitamin D3 (calcitriol) in the human keratinocyte line HaCaT. Photochem Photobiol 2000, 72:803-809.
13. Lehmann B. Role of the vitamin D3 pathway in healthy and diseased skin - facts, contradictions and hypotheses. Exp Dermatol 2009, 18:97-108.
14. Reich A, Lehmann B, Meurer M, Muller D J. Structural alterations provoked by narrow band ultraviolet B in immortalized keratinocytes: assessment by atomic force microscopy. Exp Dermatol 2007, 16:1007-1015.
15. Reich A, Meurer M, Viehweg A, Muller D J. Narrow-band UVB induced externalization of selected nuclear antigens in keratinocytes: implications for lupus erythematosus pathogenesis. Photochem Photobiol 2009, 85:1-7.
16. Gloor M, Scherotzke A. Age dependence of ultraviolet light-induced erythema following narrow-band UVB exposure. Photodermatol Photoimmunol Photomed 2002, 18:121-126.
17. Aufiero B M, Talwar H, Young C. Narrow-band UVB induces apoptosis in human keratinocytes. J Photochem Photobiol B 2006, 82:132-139.
18. Punnonen K, Puntala A, Jansen C T, Ahotupa M. UVB irradiation induces lipid peroxidation and reduces antioxidant enzyme activities in human keratinocytes in vitro. Acta Derm Venereol 1991, 71:239-242.
19. Punnonen K, Puustinen T, Jansen C T. Ultraviolet B irradiation induces changes in the distribution and release of arachidonic acid, dihomo-gamma-linolenic acid, and eicosapentaenoic acid in human keratinocytes in culture. J Invest Dermatol 1987, 88:611-614.
20. Punnonen K, Yuspa S H. Ultraviolet light irradiation increases cellular diacylglycerol and induces translocation of diacylglycerol kinase in murine keratinocytes. J Invest Dermatol 1992, 99:221-226.
21. Magnoni C, Euclidi E, Benassi L. Ultraviolet B radiation induces activation of neutral and acidic sphingomyelinases and ceramide generation in cultured normal human keratinocytes. Toxicol In Vitro 2002, 16:349-355.
22. Boukamp P, Petrussevska R T, Breitcreutz D, Hornung J, Marham A, Fusenig N E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocytes cell line. J Cell Biol 1988, 106:761-771.
23. Bligh E G, Dyer W J. A rapid method for total lipid extraction and purification. Can J Biochem Physiol 1959, 37:911-917.
24. Schürer N, Köhne A, Schliep V, Barlag K, Goerz G. Lipid composition and synthesis of HaCaT cells, an immortalized human keratinocyte line, in comparison with normal human adult keratinocytes. Exp Dermatol 1993, 2:179-185.
25. Dasgupta S, Hogan E L. Chromatographic resolution and quantitative assay of CNS tissue sphingoids and sphingolipids. J Lipid Res 2001, 42:301-308.
26. Kuerschner L, Ejsing C S, Ekroos K, Shevchenko A, Anderson K I, Thiele C. Polyene-lipids: a new tool to image lipids. Nat Methods 2005, 2:39-45.
27. Schwudke D, Liebisch G, Herzog R, Schmitz G, Shevchenko A. Shotgun lipidomics by tandem mass spectrometry under data-dependent acquisition control. Methods Enzymol 2007, 433:175-191.
28. Schwudke D, Hannich J T, Surendranath V. Top-down lipidomic screens by multivariate analysis of high-resolution survey mass spectra. Anal Chem 2007, 79:4083-4093.
29. Bonzón-Kulichenko E, Schwudke D, Gallardo N. Central leptin regulates total ceramide content and sterol regulatory element binding protein-1C proteolytic maturation in rat white adipose tissue. Endocrinology 2009, 150:169-178.
30. Finstad H S, Dyrendal H, Myhrstad M C, Heimli H, Drevon C A. Uptake and activation of eicosapentaenoic acid are related to accumulation of triacylglycerol in Ramos cells dying from apoptosis. J Lipid Res 2000, 41:554-563.
31. Al-Saffar N M, Titley J C, Robertson D. Apoptosis is associated with triacylglycerol accumulation in Jurkat T-cells. Br J Cancer 2002, 86:963-970.
32. Listenberger L L, Han X, Lewis S E. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 2003, 100:3077-3082.
33. Martins de Lima T, Cury-Boaventura M F, Giannocco G, Nunes M T, Curi R. Comparative toxicity of fatty acids on a macrophage cell line (J774). Clin Sci (Lond) 2006, 111:307-317.
34. Cnop M, Hannaert J C, Hoorens A, Eizirik D L, Pipeleers D G. Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 2001, 50:1771-1777.
35. Healy D A, Watson R W, Newsholem P. Polyunsaturated and monounsaturated fatty acids increase neutral lipid accumulation, caspase activation and apoptosis in a neutrophil-like, differentiated HL-60 cell line. Clin Sci 2003, 104:171-179.
36. Williams S N O, Anthony M L, Brindle K M. Induction of apoptosis in two mammalian cell lines results in increased levels of fructose-1,6-bisphosphate and CDP-choline as determined by 31P MRS. Magn Reson Med 1998, 40:411-420.
37. Anthony M L, Zhao M, Brindle K M. Inhibition of phosphatidylcholine biosynthesis following induction of apoptosis in HL-60 cells. J Biol Chem 1999, 274:19686-19692.
38. Iturralde M, Gamen S, Pardo J. Saturated free fatty acid release and intracellular ceramide generation during apoptosis induction are closely related processes. Biochim Biophys Acta 2003, 1634:40-51.
39. Aronis A, Madar Z, Tirosh O. Mechanism of underlying oxidative stress-mediated lipotoxicity: exposure of J744.2 macrophages to triacylglycerols facilitates mitochondrial reactive oxygen species production and cellular necrosis. Free Radical Biol Med 2005, 38:1221-1230.
40. Schmuth M, Haqq CM, Cairns WJ. Peroxisome proliferator-activated receptor (PPAR)-beta/delta stimulates differentiation and lipid accumulation in keratinocytes. J Invest Dermatol 2004, 122:971-983.
41. Mathias S, Pena L A, Kolesnick R N. Signal transduction of stress via ceramide. Biochem J 1998, 335:465-480.
42. Pena L A, Fuks Z, Kolesnick R. Stress-induced apoptosis and the sphingomyelin pathway. Biochem Pharmacol 1997, 53:615-621.
43. Perry D K, Carton J, Shah A K, Meredith F, Uhlinger D J, Hannun Y A. Serine palmitoyltrasferase regultes de novo ceramide generation during etoposide-induced apoptosis. J Biol Chem 2000, 275:9078-9084.
44. Uchida Y, Di Nardo A, Collins V, Elias P M, Holleran W M. De novo ceramide synthesis participates in the ultraviolet B irradiation-induced apoptosis in undifferentiated cultured human keratinocytes. J Invest Dermatol 2003, 120:662-669.
45. Magnoni C, Euclidi E, Benassi L. Ultraviolet B radiation induces activation of neutral and acidic sphingomyelinases and ceramide generation in cultured normal human keratinocytes. Toxicol in Vitro 2002, 16:349-355.
46. Verdonck LF, van Heugten HG. Ether lipids are effective cytotoxic drugs against multidrug-resistant acute leukemia cells and can act by the induction of apoptosis. Leuk Res 1997, 21:37-43.
47. Cabaner C, Gajate C, Macho A, Muñoz E, Modolell M, Mollinedo F. Induction of apoptosis in human mitogen-activated peripheral blood T-lymphocytes by the ether phospholipid ET-18-OCH3: involvement of the Fas receptor/ligand system. Br J Pharmacol 1999, 127:813-825.
48. Carsberg CJ, Ohanian J, Friedmann PS. Ultraviolet radiation stimulates a biphasic pattern of 1,2-diacylglycerol formation in cultured human melanocytes and keratinocytes by activation of phospholipases C and D. Biochem J 1995, 305:471-477.
49. Gordon PR, Gilchrest BA. Human melanogenesis is stimulated by diacylglycerol. J Invest Dermatol 1989, 93:700-702.
50. Choi MJ, Maibach HI. Role of ceramides in barrier function of healthy and diseased skin. Am J Clin Dermatol 2005, 6:215-223.
51. Chamlin SL, Kao J, Frieden IJ. Ceramide-dominant barrier repair lipids alleviate childhood atopic dermatitis: changes in barrier function provide a sensitive indicator of disease activity. J Am Acad Dermatol 2002, 47:198-208.
52. Wefers H, Melnik BC, Flür M, Bluhm C, Lehmann P, Plewig G. Influence of UV irradiation on the composition of human stratum corneum lipids. J Invest Dermatol 1991, 96:959-962.