Visualization by mass spectrometry of 2-dimensional changes in rat brain lipids, including N-acylphosphatidylethanolamines, during neonatal brain ischemia

FASEB Journal

Volumn 26, Issue 6, 2012, Pages 2667-2673

  Janfelt, Christian ^a   Wellner, Niels ^a   Leger, Pierre Louis ^b   Kokesch Himmelreich, Julia ^c   Hansen, Steen Honoré ^a   Charriaut Marlangue, Christiane ^b   Hansen, Harald Severin ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b INSERM   (France)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Arachidonic acid; Desorption electrospray ionization; Docosahexaenoic acid; Free fatty acids; N palmitoylethanolamine; Sodium potassium pump

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; LIPID; LYSOPHOSPHATIDYLCHOLINE; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPID; POTASSIUM; SODIUM;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CAROTID ARTERY OBSTRUCTION; CONTROLLED STUDY; ELECTROCOAGULATION; ELECTROSPRAY MASS SPECTROMETRY; LIPID BRAIN LEVEL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN CHEMISTRY; BRAIN ISCHEMIA; ETHANOLAMINES; FATTY ACIDS, NONESTERIFIED; FEMALE; INFARCTION, MIDDLE CEREBRAL ARTERY; LIPIDS; MALE; PHOSPHATIDYLETHANOLAMINES; PLASMALOGENS; RATS; RATS, WISTAR; REPERFUSION INJURY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

ANIMALIA; RATTUS;

EID: 84861762663     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-201152     Document Type: Article

References (54)

1. Guan, X. L., He, X., Ong, W. Y., Yeo, W. K., Shui, G., and Wenk, M. R. (2006) Non-targeted profiling of lipids during kainate-induced neuronal injury. FASEB J. 20, 1152-1161 (Pubitemid 44943911)
2. Moesgaard, B., Jaroszewski, J. W., and Hansen, H. S. (1999) Accumulation of N-acyl-ethanolamine phospholipids in rat brains during post-decapitative ischemia: a 31P NMR study. J. Lipid Res. 40, 515-521 (Pubitemid 29116155)
3. Natarajan, V, Schmid, P. C., and Schmid, H. H. O. (1986) N-Acylethanolamine phospholipid metabolism in normal and ischemic rat brain. Biochim. Biophys. Acta 878, 32-41 (Pubitemid 16049127)
4. Hansen, H. H., Schmid, P. C., Bittigau, P., Lastres-Becker, I., Berrendero, F., Manzanares, J., Ikonomidou, C., Schmid, H. H. O., Feŕnandez-Ruiz, J. J., and Hansen, H. S. (2001) Anandamide, but not 2-arachidonoylglycerol, accumulates during in vivo neurodegeneration. J. Neurochem. 78, 1415-1427 (Pubitemid 32899773)
5. Hansen, H. H., Ikonomidou, C., Bittigau, P., Hansen, S. H., and Hansen, H. S. (2001) Accumulation of the anandamide precursor and other N-acylethanolamine phospholipids in infant rat models of in vivo necrotic and apoptotic neuronal death. J. Neurochem. 76, 39-46 (Pubitemid 32044366)
6. Hansen, H. S., Moesgaard, B., Petersen, G., and Hansen, H. H. (2002) Putative neuroprotective actions of N-acyl-ethanolamines. Pharmacol. Ther. 95, 119-126 (Pubitemid 35232130)
7. Hansen, H. S., Moesgaard, B., Hansen, H. H., and Petersen, G. (2000) N-Acylethanolamines and precursor phospholipids - relation to cell injury. Chem. Phys. Lipids 108, 135-150
8. Di Marzo, V., Fontana, A., Cadas, H., Schinelli, S., Cimino, G., Schwartz, J.-C., and Piomelli, D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372, 686-691
9. Hansen, H. S., Lauritzen, L., Strand, A. M., Vinggaard, A. M., Frandsen, A., and Schousboe, A. (1997) Characterization of glutamate-induced formation of N-acylphosphatidylethanolamine and N-acylethanolamine in cultured neocortical neurons. J. Neurochem. 69, 753-761 (Pubitemid 27327979)
10. Alger, B. E., and Kim, J. (2011) Supply and demand for endocannabinoids. Trends Neurosci. 34, 304-315
11. Tsuboi, K., Okamoto, Y., Ikematsu, N., Inoue, M., Shimizu, Y., Uyama, T., Wang, J., Deutsch, D. G., Burns, M. P., Ulloa, N. M., Tokumura, A., and Ueda, N. (2011) Enzymatic formation of N-acylethanolamines from N-acylethanolamine plasmalogen through N-acylphosphatidylethanolamine-hydrolyzing phospholipase D-dependent and -independent pathways. Biochim. Biophys. Acta 1811, 565-577
12. Rodriguez de Fonseca, F., Navarro, M., Gómez, R., Escuredo, L., Nava, F., Fu, J., Murillo-Rodríguez, E., Giuffrida, A., LoVerme, J., Gaetani, S., Kathuria, S., Gall, C., and Piomelli, D. (2001) An anorexic lipid mediator regulated by feeding. Nature 414, 209-212 (Pubitemid 33051235)
13. Diep, T. A., Madsen, A. N., Holst, B., Kristiansen, M. M., Wellner, N., Hansen, S. H., and Hansen, H. S. (2011) Dietary fat decreases intestinal levels of the anorectic lipids through a fat sensor. FASEB J. 25, 765-774
14. Schomacher, M., Muller, H. D., Sommer, C., Schwab, S., and Schabitz, W. R. (2008) Endocannabinoids mediate neuroprotection after transient focal cerebral ischemia. Brain Res. 1240, 213-220
15. Garg, P., Duncan, R. S., Kaja, S., and Koulen, P. (2010) Intracellular mechanisms of N-acylethanolamine-mediated neuroprotection in a rat model of stroke. Neuroscience 166, 252-262
16. Kilaru, A., Tamura, P., Garg, P., Isaac, G., Baxter, D., Duncan, R.S., Welti, R., Koulen, P., Chapman, K. D., and Venables, B. J. (2010) Changes in N-acylethanolamine pathway related metabolites in a rat model of cerebral ischemia/reperfusion. J. Glycom. Lipidom. 1, 101
17. Esposito, E., Paterniti, I., Mazzon, E., Genovese, T., Di Paola, R., Galuppo, M., and Cuzzocrea, S. Effects of palmitoylethanolamide on release of mast cell peptidases and neurotrophic factors after spinal cord injury. Brain Behav. Immun. 25, 1099-1112, 2011
18. Gillum, M. P., Zhang, D., Zhang, X. M., Erion, D. M., Jamison, R. A., Choi, C., Dong, J., Shanabrough, M., Duenas, H. R., Frederick, D. W., Hsiao, J. J., Horvath, T. L., Lo, C. M., Tso, P., Cline, G. W., and Shulman, G. I. (2008) N-acylphosphatidylethanolamine, a gut- derived circulating factor induced by fat ingestion, inhibits food intake. Cell 135, 813-824
19. Wellner, N., Tsuboi, K., Madsen, A. N., Holst, B., Diep, T. A., Nakao, M., Tokumura, A., Burns, M. P., Deutsch, D. G., Ueda, N., and Hansen, H. S. (2011) Studies on the anorectic effect of N-acylphosphatidylethanolamine and phosphatidylethanolamine in mice. Biochim. Biophys. Acta 1811, 508-512
20. Coulon, D., Faure, L., Salmon, M., Wattelet, V., and Bessoule, J. J. (2012) Occurrence, biosynthesis and functions of N-acylphosphatidylethanolamines (NAPE): Not just precursors of N-acylethanolamines (NAE). Biochimie (Paris) 94, 75-85
21. Ong, W. Y., Farooqui, T., and Farooqui, A. A. (2010) Involvement of cytosolic phospholipase A(2), calcium independent phospholipase A(2) and plasmalogen selective phospholipase A(2) in neurodegenerative and neuropsychiatric conditions. Curr. Med. Chem. 17, 2746-2763
22. Belayev, L., Khoutorova, L., Atkins, K. D., Eady, T. N., Hong, S., Lu, Y., Obenaus, A., and Bazan, N. G. (2011) Docosahexaenoic acid therapy of experimental ischemic stroke. Transl. Stroke Res. 2, 33-41
23. Ji, R. R., Xu, Z. Z., Strichartz, G., and Serhan, C. N. (2011) Emerging roles of resolvins in the resolution of inflammation and pain. Trends Neurosci. 34, 599-609
24. Hansen, H. S. (2010) Palmitoylethanolamide and other anandamide congeners. Proposed role in the diseased brain. Exp. Neurol. 224, 48-55
25. Goto-Inoue, N., Hayasaka, T., Zaima, N., and Setou, M. (2011) Imaging mass spectrometry for lipidomics. Biochim. Biophys. Acta 1811, 961-969
26. Murphy, R. C., and Gaskell, S. (2011) J. New applications of mass spectrometry in lipid analysis. J. Biol. Chem. 286, 25427-25433
27. Moesgaard, B., Petersen, G., Jaroszewski, J. W., and Hansen, H. S. (2000) Age dependent accumulation of N-acyl-ethanolamine phospholipids in ischemic rat brain. A (31)P NMR and enzyme activity study. J. Lipid Res. 41, 985-990 (Pubitemid 30434330)
28. Takats, Z., Wiseman, J.M., Gologan, B., and Cooks, R.G. (2004) Mass spectrometry sampling under ambient conditions with desorption electrospray ionization. Science 306, 471-473 (Pubitemid 39372443)
29. Wiseman, J. M., Ifa, D. R., Song, Q., and Cooks, R. G. (2006) Tissue imaging at atmospheric pressure using desorption electrospray ionization (DESI) mass spectrometry. Angew. Chem. Int. Ed. Engl. 45, 7188-7192 (Pubitemid 44748295)
30. Bonnin, P., Leger, P. L., Deroide, N., Fau, S., Baud, O., Pocard, M., Charriaut-Marlangue, C., and Renolleau. S. (2011) Impact of intracranial blood-flow redistribution on stroke size during ischemia-reperfusion in 7-day-old rats. J. Neurosci. Methods 198, 103-109
31. Thunig, J., Hansen, S. H., and Janfelt, C. (2011) Analysis of secondary plant metabolites by indirect desorption electrospray ionization imaging mass spectrometry. Anal. Chem. 83, 3256-3259
32. Koizumi, S., Yamamoto, S., Hayasaka, T., Konishi, Y., Yamaguchi-Okada, M., Goto-Inoue, N., Sugiura, Y., Setou, M., and Namba, H. (2010) Imaging mass spectrometry revealed the production of lyso-phosphatidylcholine in the injured ischemic rat brain. Neuroscience 168, 219-225
33. Hankin, J. A., Farias, S. E., Barkley, R. M., Heidenreich, K. A., Frey, L. C., Hamazaki, K., Kim, H.-Y., and Murphy, R. C. (2011) MALDI mass spectrometric imaging of lipids in rat brain injury models. J. Am. Soc. Mass Spectrom. 22, 1014-1021
34. Saito, M., Chakraborty, G., Hegde, M., Ohsie, J., Paik, S. M., Vadasz, C., and Saito, M. (2010) Involvement of ceramide in ethanol-induced apoptotic neurodegeneration in the neonatal mouse brain. J. Neurochem. 115, 168-177
35. Franklin, A., Parmentier-Batteur, S., Walter, L., Greenberg, D. A., and Stella, N. (2003) Palmitoylethanolamide increases after focal cerebral ischemia and potentiates microglial cell motility. J. Neurosci. 23, 7767-7775 (Pubitemid 37052344)
36. Degn, M., Lambertsen, K. L., Petersen, G., Meldgaard, M., Artmann, A., Clausen, B. H., Hansen, S. H., Finsen, B., Hansen, H. S., and Lund, T. M. (2007) Changes in brain levels of N-acylethanolamines and 2-arachidonoylglycerol in focal cerebral ischemia in mice. J. Neurochem. 103, 1907-1916 (Pubitemid 350126623)
37. Berger, C., Schmid, P. C., Schabitz, W. R., Wolf, M., Schwab, S., and Schmid, H. H. O. (2004) Massive accumulation of N-acylethanolamines after stroke. Cell signalling in acute cerebral ischemia? J. Neurochem. 88, 1159-1167 (Pubitemid 38280683)
38. Terova, B., Petersen, G., Hansen, H. S., and Slotte, J. P. (2005) N-acyl phosphatidylethanolamines affect the lateral distribution of cholesterol in membranes. Biochim. Biophys. Acta 1715, 49-56 (Pubitemid 41161159)
39. Swamy, M. J., Tarafdar, P. K., and Kamlekar, R. K. (2010) Structure, phase behaviour and membrane interactions of N-acylethanolamines and N-acylphosphatidylethanolamines. Chem. Phys. Lipids 163, 266-279
40. Maccarrone, M., Gasperi, V., Catani, M. V., Diep, T. A., Dainese, E., Hansen, H. S., and Avigliano, L. (2010) The endocannabinoid system and its relevance for nutrition. Annu. Rev. Nutr. 30, 423-440
41. Muthian, S., Rademacher, D. J., Roelke, C. T., Gross, G. J., and Hillard, C. J. (2004) Anandamide content is increased and Cb1 cannabinoid receptor blockade is protective during transient, focal cerebral ischemia. Neuroscience 129, 743-750 (Pubitemid 39487125)
42. Sinor, A. D., Irvin, S. M., and Greenberg, D. A. (2000) Endocannabinoids protect cerebral cortical neurons from in vitro ischemia in rats. Neurosc.i Lett. 278, 157-160 (Pubitemid 30009481)
43. Sun, Y, Alexander, S. P., Garle, M. J., Gibson, C. L., Hewitt, K., Murphy, S. P., Kendall, D. A., and Bennett, A. J. (2007) Cannabinoid activation of PPARalpha; a novel neuroprotective mechanism. Br. J. Pharmacol. 152, 734-743 (Pubitemid 350034991)
44. Van der Stelt, M., Veldhuis, W. B., Van Haaften, G. W., Fezza, F., Bisogno, T., Bär, P. R., Veldink, G. A., Vliegenthart, J. F. G., Di Marzo, V., and Nicolay, K. (2001) Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J. Neurosci. 21, 8765-8771 (Pubitemid 33054840)
45. Galan-Rodriguez, B., Suarez, J., Gonzalez-Aparicio, R., Bermudez- Silva, F. J., Maldonado, R., Robledo, P., Rodriguez de Fonseca, F., and Fernandez-Espejo, E. (2009) Oleoylethanolamide exerts partial and dose-dependent neuroprotection of substantia nigra dopamine neurons. Neuropharmacol. 56, 653-664
46. Panikashvili, D., Simeonidou, C., Ben-Shabat, S., Hanus, L., Breuer, A., Mechoulam, R., and Shohami, E. (2001) An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413, 527-531 (Pubitemid 32938751)
47. Murikinati, S., Juttler, E., Keinert, T., Ridder, D. A., Muhammad, S., Waibler, Z., Ledent, C., Zimmer, A., Kalinke, U., and Schwaninger, M. (2010) Activation of cannabinoid 2 receptors protects against cerebral ischemia by inhibiting neutrophil recruitment. FASEB J. 24, 788-798
48. Bazan, N. G. (1970) Effects of ischemia and electroconvulsive shock on free fatty acid pool in the brain. Biochim. Biophys. Acta 218, 1-10
49. Deutsch, J., Rapoport, S. I., and Purdon, A. D. (1997) Relation between free fatty acid and acyl-CoA concentrations in rat brain following decapitation. Neurochem. Res. 22, 759-765 (Pubitemid 27300632)
50. 2 in ischemic and toxic brain injury. Neurochem. Res. 25, 745-753
51. Nomura, D. K., Morrison, B. E., Blankman, J. L., Long, J. Z., Kinsey, S. G., Marcondes, M. C., Ward, A. M., Hahn, Y. K., Lichtman, A. H., Conti, B., and Cravatt, B. F. (2011) Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science 334, 809-813
52. Manicke, N. E., Dill, A. L., Ifa, D. R., and Cooks, R. G. (2010) High-resolution tissue imaging on an orbitrap mass spectrometer by desorption electrospray ionization mass spectrometry. J. Mass Spectrom. 45, 223-226
53. Chen, C. T., Ma, D. W., Kim, J. H., Mount, H. T., and Bazinet, R. P. (2008) The low density lipoprotein receptor is not necessary for maintaining mouse brain polyunsaturated fatty acid concentrations. J. Lipid Res. 49, 147-152
54. Harkewicz, R., Fahy, E., Andreyev, A., and Dennis, E.A. (2007) Arachidonate-derived dihomoprostaglandin production observed in endotoxin-stimulated macrophage-like cells. J. Biol. Chem. 282, 2899-2910 (Pubitemid 47084335)