Abstract
It has long been known that N-acylethanolamine phospholipids [N-acylphosphatidylethanolamine (N-acyl PE)] and N-acylethanolamines (NAEs) accumulate in mammalian tissues undergoing degenerative membrane changes associated with necrosis. Here we studied the effects of stress factors (UVB irradiation and serum deprivation) on the endogenous levels of N-acyl PE and NAE in mouse epidermal JB6 P(+) cells. We found that 16:0, 18:0, 18:1,n-9 and 18:1,n-7 are the predominant amide-linked fatty acids in both N-acyl PE and NAE in these cells. UVB irradiation and serum deprivation resulted in significantly increased levels of N-acyl PE and NAE, especially 18:1, n-9 N-acyl PE and NAE. UVB challenge increased the cellular content of anandamide (20:4,n-6 NAE), but this increase was the lowest of all NAEs measured. Serum deprivation resulted in a decreased cellular anandamide level, as well as a decrease in 20:4,n-6 N-acyl PE. Interestingly, the replacement of serum-free medium with medium containing 5% (v/v) fetal calf serum after 36 h of serum deprivation restored N-acyl PE and NAE levels almost completely within 4-8 h. These data suggest the involvement of N-acyl PE and NAE in cellular responses to stress.
Full Text
The Full Text of this article is available as a PDF (135.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ambrosini A., Bertoli E., Mariani P., Tanfani F., Wozniak M., Zolese G. N-acylethanolamines as membrane topological stress compromising agents. Biochim Biophys Acta. 1993 Jun 5;1148(2):351–355. doi: 10.1016/0005-2736(93)90149-t. [DOI] [PubMed] [Google Scholar]
- BARTLETT G. R. Phosphorus assay in column chromatography. J Biol Chem. 1959 Mar;234(3):466–468. [PubMed] [Google Scholar]
- BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
- Chen N., Ma W. y., Huang C., Dong Z. Translocation of protein kinase Cepsilon and protein kinase Cdelta to membrane is required for ultraviolet B-induced activation of mitogen-activated protein kinases and apoptosis. J Biol Chem. 1999 May 28;274(22):15389–15394. doi: 10.1074/jbc.274.22.15389. [DOI] [PubMed] [Google Scholar]
- Derocq J. M., Bouaboula M., Marchand J., Rinaldi-Carmona M., Ségui M., Casellas P. The endogenous cannabinoid anandamide is a lipid messenger activating cell growth via a cannabinoid receptor-independent pathway in hematopoietic cell lines. FEBS Lett. 1998 Apr 3;425(3):419–425. doi: 10.1016/s0014-5793(98)00275-0. [DOI] [PubMed] [Google Scholar]
- Devane W. A., Hanus L., Breuer A., Pertwee R. G., Stevenson L. A., Griffin G., Gibson D., Mandelbaum A., Etinger A., Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science. 1992 Dec 18;258(5090):1946–1949. doi: 10.1126/science.1470919. [DOI] [PubMed] [Google Scholar]
- Devary Y., Gottlieb R. A., Lau L. F., Karin M. Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol Cell Biol. 1991 May;11(5):2804–2811. doi: 10.1128/mcb.11.5.2804. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Di Marzo V. 'Endocannabinoids' and other fatty acid derivatives with cannabimimetic properties: biochemistry and possible physiopathological relevance. Biochim Biophys Acta. 1998 Jun 15;1392(2-3):153–175. doi: 10.1016/s0005-2760(98)00042-3. [DOI] [PubMed] [Google Scholar]
- Di Marzo V., Fontana A., Cadas H., Schinelli S., Cimino G., Schwartz J. C., Piomelli D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature. 1994 Dec 15;372(6507):686–691. doi: 10.1038/372686a0. [DOI] [PubMed] [Google Scholar]
- Ding M., Li J. J., Leonard S. S., Ye J. P., Shi X., Colburn N. H., Castranova V., Vallyathan V. Vanadate-induced activation of activator protein-1: role of reactive oxygen species. Carcinogenesis. 1999 Apr;20(4):663–668. doi: 10.1093/carcin/20.4.663. [DOI] [PubMed] [Google Scholar]
- Domingo J. C., Mora M., Africa de Madariaga M. Incorporation of N-acylethanolamine phospholipids into egg phosphatidylcholine vesicles: characterization and permeability properties of the binary systems. Biochim Biophys Acta. 1993 Jun 5;1148(2):308–316. doi: 10.1016/0005-2736(93)90144-o. [DOI] [PubMed] [Google Scholar]
- Dong Z., Ma W., Huang C., Yang C. S. Inhibition of tumor promoter-induced activator protein 1 activation and cell transformation by tea polyphenols, (-)-epigallocatechin gallate, and theaflavins. Cancer Res. 1997 Oct 1;57(19):4414–4419. [PubMed] [Google Scholar]
- Dérijard B., Hibi M., Wu I. H., Barrett T., Su B., Deng T., Karin M., Davis R. J. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell. 1994 Mar 25;76(6):1025–1037. doi: 10.1016/0092-8674(94)90380-8. [DOI] [PubMed] [Google Scholar]
- Epps D. E., Natarajan V., Schmid P. C., Schmid H. O. Accumulation of N-acylethanolamine glycerophospholipids in infarcted myocardium. Biochim Biophys Acta. 1980 Jun 23;618(3):420–430. doi: 10.1016/0005-2760(80)90260-x. [DOI] [PubMed] [Google Scholar]
- Epps D. E., Palmer J. W., Schmid H. H., Pfeiffer D. R. Inhibition of permeability-dependent Ca2+ release from mitochondria by N-acylethanolamines, a class of lipids synthesized in ischemic heart tissue. J Biol Chem. 1982 Feb 10;257(3):1383–1391. [PubMed] [Google Scholar]
- Epps D. E., Schmid P. C., Natarajan V., Schmid H. H. N-Acylethanolamine accumulation in infarcted myocardium. Biochem Biophys Res Commun. 1979 Sep 27;90(2):628–633. doi: 10.1016/0006-291x(79)91281-6. [DOI] [PubMed] [Google Scholar]
- Felder C. C., Briley E. M., Axelrod J., Simpson J. T., Mackie K., Devane W. A. Anandamide, an endogenous cannabimimetic eicosanoid, binds to the cloned human cannabinoid receptor and stimulates receptor-mediated signal transduction. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7656–7660. doi: 10.1073/pnas.90.16.7656. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Giuffrida A., Piomelli D. Isotope dilution GC/MS determination of anandamide and other fatty acylethanolamides in rat blood plasma. FEBS Lett. 1998 Feb 6;422(3):373–376. doi: 10.1016/s0014-5793(98)00046-5. [DOI] [PubMed] [Google Scholar]
- Hannun Y. A. Functions of ceramide in coordinating cellular responses to stress. Science. 1996 Dec 13;274(5294):1855–1859. doi: 10.1126/science.274.5294.1855. [DOI] [PubMed] [Google Scholar]
- Hansen H. S., Lauritzen L., Strand A. M., Moesgaard B., Frandsen A. Glutamate stimulates the formation of N-acylphosphatidylethanolamine and N-acylethanolamine in cortical neurons in culture. Biochim Biophys Acta. 1995 Oct 5;1258(3):303–308. doi: 10.1016/0005-2760(95)00134-x. [DOI] [PubMed] [Google Scholar]
- Hansen H. S., Lauritzen L., Strand A. M., Vinggaard A. M., Frandsen A., Schousboe A. Characterization of glutamate-induced formation of N-acylphosphatidylethanolamine and N-acylethanolamine in cultured neocortical neurons. J Neurochem. 1997 Aug;69(2):753–761. doi: 10.1046/j.1471-4159.1997.69020753.x. [DOI] [PubMed] [Google Scholar]
- Hanus L., Gopher A., Almog S., Mechoulam R. Two new unsaturated fatty acid ethanolamides in brain that bind to the cannabinoid receptor. J Med Chem. 1993 Oct 1;36(20):3032–3034. doi: 10.1021/jm00072a026. [DOI] [PubMed] [Google Scholar]
- Huang C., Ma W. Y., Dong Z. The extracellular-signal-regulated protein kinases (Erks) are required for UV-induced AP-1 activation in JB6 cells. Oncogene. 1999 May 6;18(18):2828–2835. doi: 10.1038/sj.onc.1202639. [DOI] [PubMed] [Google Scholar]
- Huang C., Ma W. Y., Li J., Dong Z. Arsenic induces apoptosis through a c-Jun NH2-terminal kinase-dependent, p53-independent pathway. Cancer Res. 1999 Jul 1;59(13):3053–3058. [PubMed] [Google Scholar]
- Huang C., Ma W. y., Ding M., Bowden G. T., Dong Z. Direct evidence for an important role of sphingomyelinase in ultraviolet-induced activation of c-Jun N-terminal kinase. J Biol Chem. 1997 Oct 31;272(44):27753–27757. doi: 10.1074/jbc.272.44.27753. [DOI] [PubMed] [Google Scholar]
- Huang C., Schmid P. C., Ma W. Y., Schmid H. H., Dong Z. Phosphatidylinositol-3 kinase is necessary for 12-O-tetradecanoylphorbol-13-acetate-induced cell transformation and activated protein 1 activation. J Biol Chem. 1997 Feb 14;272(7):4187–4194. doi: 10.1074/jbc.272.7.4187. [DOI] [PubMed] [Google Scholar]
- Kondo S., Sugiura T., Kodaka T., Kudo N., Waku K., Tokumura A. Accumulation of various N-acylethanolamines including N-arachidonoylethanolamine (anandamide) in cadmium chloride-administered rat testis. Arch Biochem Biophys. 1998 Jun 15;354(2):303–310. doi: 10.1006/abbi.1998.0688. [DOI] [PubMed] [Google Scholar]
- Mercadal M., Domingo J. C., Bermudez M., Mora M., De Madariaga M. A. N-palmitoylphosphatidylethanolamine stabilizes liposomes in the presence of human serum: effect of lipidic composition and system characterization. Biochim Biophys Acta. 1995 May 4;1235(2):281–288. doi: 10.1016/0005-2736(95)80015-8. [DOI] [PubMed] [Google Scholar]
- Natarajan V., Reddy P. V., Schmid P. C., Schmid H. H. N-Acylation of ethanolamine phospholipids in canine myocardium. Biochim Biophys Acta. 1982 Aug 18;712(2):342–355. doi: 10.1016/0005-2760(82)90352-6. [DOI] [PubMed] [Google Scholar]
- Natarajan V., Schmid P. C., Schmid H. H. N-acylethanolamine phospholipid metabolism in normal and ischemic rat brain. Biochim Biophys Acta. 1986 Aug 14;878(1):32–41. doi: 10.1016/0005-2760(86)90341-3. [DOI] [PubMed] [Google Scholar]
- Newman J. L., Stiers D. L., Anderson W. H., Schmid H. H. Phase behavior of synthetic N-acylethanolamine phospholipids. Chem Phys Lipids. 1986 Dec 31;42(4):249–260. doi: 10.1016/0009-3084(86)90084-8. [DOI] [PubMed] [Google Scholar]
- Reddy P. V., Schmid P. C., Natarajan V., Muramatsu T., Schmid H. H. Properties of canine myocardial phosphatidylethanolamine N-acyltransferase. Biochim Biophys Acta. 1984 Aug 15;795(1):130–136. doi: 10.1016/0005-2760(84)90113-9. [DOI] [PubMed] [Google Scholar]
- Schmid H. H., Schmid P. C., Natarajan V. N-acylated glycerophospholipids and their derivatives. Prog Lipid Res. 1990;29(1):1–43. doi: 10.1016/0163-7827(90)90004-5. [DOI] [PubMed] [Google Scholar]
- Schmid P. C., Krebsbach R. J., Perry S. R., Dettmer T. M., Maasson J. L., Schmid H. H. Occurrence and postmortem generation of anandamide and other long-chain N-acylethanolamines in mammalian brain. FEBS Lett. 1995 Nov 13;375(1-2):117–120. doi: 10.1016/0014-5793(95)01194-j. [DOI] [PubMed] [Google Scholar]
- Schmid P. C., Kuwae T., Krebsbach R. J., Schmid H. H. Anandamide and other N-acylethanolamines in mouse peritoneal macrophages. Chem Phys Lipids. 1997 Jul 14;87(2):103–110. doi: 10.1016/s0009-3084(97)00032-7. [DOI] [PubMed] [Google Scholar]
- Schmid P. C., Natarajan V., Weis B. K., Schmid H. H. Hydrolysis of N-acylated glycerophospholipids by phospholipases A2 and D: a method of identification and analysis. Chem Phys Lipids. 1986 Oct-Nov;41(3-4):195–207. doi: 10.1016/0009-3084(86)90022-8. [DOI] [PubMed] [Google Scholar]
- Schmid P. C., Reddy P. V., Natarajan V., Schmid H. H. Metabolism of N-acylethanolamine phospholipids by a mammalian phosphodiesterase of the phospholipase D type. J Biol Chem. 1983 Aug 10;258(15):9302–9306. [PubMed] [Google Scholar]
- Schmid P. C., Schwindenhammer D., Krebsbach R. J., Schmid H. H. Alternative pathways of anandamide biosynthesis in rat testes. Chem Phys Lipids. 1998 Mar;92(1):27–35. doi: 10.1016/s0009-3084(97)00109-6. [DOI] [PubMed] [Google Scholar]
- Skaper S. D., Buriani A., Dal Toso R., Petrelli L., Romanello S., Facci L., Leon A. The ALIAmide palmitoylethanolamide and cannabinoids, but not anandamide, are protective in a delayed postglutamate paradigm of excitotoxic death in cerebellar granule neurons. Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3984–3989. doi: 10.1073/pnas.93.9.3984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spinedi A., Di Bartolomeo S., Piacentini M. N-Oleoylethanolamine inhibits glucosylation of natural ceramides in CHP-100 neuroepithelioma cells: possible implications for apoptosis. Biochem Biophys Res Commun. 1999 Feb 16;255(2):456–459. doi: 10.1006/bbrc.1999.0230. [DOI] [PubMed] [Google Scholar]
- Staberg B., Wulf H. C., Klemp P., Poulsen T., Brodthagen H. The carcinogenic effect of UVA irradiation. J Invest Dermatol. 1983 Dec;81(6):517–519. doi: 10.1111/1523-1747.ep12522855. [DOI] [PubMed] [Google Scholar]
- Stein B., Rahmsdorf H. J., Steffen A., Litfin M., Herrlich P. UV-induced DNA damage is an intermediate step in UV-induced expression of human immunodeficiency virus type 1, collagenase, c-fos, and metallothionein. Mol Cell Biol. 1989 Nov;9(11):5169–5181. doi: 10.1128/mcb.9.11.5169. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strickland P. T. Photocarcinogenesis by near-ultraviolet (UVA) radiation in Sencar mice. J Invest Dermatol. 1986 Aug;87(2):272–275. doi: 10.1111/1523-1747.ep12696669. [DOI] [PubMed] [Google Scholar]
- Sugita M., Willians M., Dulaney J. T., Moser H. W. Ceramidase and ceramide synthesis in human kidney and cerebellum. Description of a new alkaline ceramidase. Biochim Biophys Acta. 1975 Jul 22;398(1):125–131. doi: 10.1016/0005-2760(75)90176-9. [DOI] [PubMed] [Google Scholar]
- Sugiura T., Kondo S., Sukagawa A., Tonegawa T., Nakane S., Yamashita A., Ishima Y., Waku K. Transacylase-mediated and phosphodiesterase-mediated synthesis of N-arachidonoylethanolamine, an endogenous cannabinoid-receptor ligand, in rat brain microsomes. Comparison with synthesis from free arachidonic acid and ethanolamine. Eur J Biochem. 1996 Aug 15;240(1):53–62. doi: 10.1111/j.1432-1033.1996.0053h.x. [DOI] [PubMed] [Google Scholar]
- Sugiura T., Kondo S., Sukagawa A., Tonegawa T., Nakane S., Yamashita A., Waku K. Enzymatic synthesis of anandamide, an endogenous cannabinoid receptor ligand, through N-acylphosphatidylethanolamine pathway in testis: involvement of Ca(2+)-dependent transacylase and phosphodiesterase activities. Biochem Biophys Res Commun. 1996 Jan 5;218(1):113–117. doi: 10.1006/bbrc.1996.0020. [DOI] [PubMed] [Google Scholar]
- Valk P., Verbakel S., Vankan Y., Hol S., Mancham S., Ploemacher R., Mayen A., Löwenberg B., Delwel R. Anandamide, a natural ligand for the peripheral cannabinoid receptor is a novel synergistic growth factor for hematopoietic cells. Blood. 1997 Aug 15;90(4):1448–1457. [PubMed] [Google Scholar]
- Verheij M., Bose R., Lin X. H., Yao B., Jarvis W. D., Grant S., Birrer M. J., Szabo E., Zon L. I., Kyriakis J. M. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 1996 Mar 7;380(6569):75–79. doi: 10.1038/380075a0. [DOI] [PubMed] [Google Scholar]
