Reduction of ischemic brain injury by administration of palmitoylethanolamide after transient middle cerebral artery occlusion in rats

Brain Research

Volumn 1477, Issue , 2012, Pages 45-58

  Ahmad, Akbar ^a   Genovese, Tiziana ^a   Impellizzeri, Daniela ^a   Crupi, Rosalia ^a   Velardi, Enrico ^b   Marino, Angela ^c   Esposito, Emanuela ^a   Cuzzocrea, Salvatore ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

^c UNIVERSITY OF MESSINA   (Italy)

Author keywords

Apoptosis; Cerebral ischemia; Inflammation; Neuronal death; Nitrotyrosine; NO

Indexed keywords

3 NITROTYROSINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CHYMASE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; PALMIDROL; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN BAX; PROTEIN BCL 2; STRESS ACTIVATED PROTEIN KINASE; TRIPHENYLTETRAZOLIUM; TRYPTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN EDEMA; BRAIN FUNCTION; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN TISSUE; CELL ACTIVATION; CELL INFILTRATION; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFICACY; ENZYME DEGRADATION; ENZYME INHIBITION; HEMISPHERE; HISTOLOGY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MALE; MAST CELL; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STAINING; WHITE MATTER;

ANIMALS; ASTROCYTES; BRAIN INJURIES; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; ETHANOLAMINES; GLIAL FIBRILLARY ACIDIC PROTEIN; INFARCTION, MIDDLE CEREBRAL ARTERY; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; NEUROPROTECTIVE AGENTS; NITRIC OXIDE SYNTHASE TYPE II; PALMITIC ACIDS; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, WISTAR; REPERFUSION INJURY; TETRAZOLIUM SALTS; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA; MUS; RATTUS;

EID: 84866385818     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.08.006     Document Type: Article

References (80)

1. ArunaDevi Neuroprotective effect of 5,7,3′,4′,5′- pentahydroxy dihydroflavanol-3-O-(2″-O-galloyl)-beta-D-glucopyranoside, a polyphenolic compound in focal cerebral ischemia in rat Eur. J. Pharmacol 2010
2. R. ArunaDevi Neuroprotective effect of s-methylisothiourea in transient focal cerebral ischemia in rat Nitric Oxide 22 2010 1 10
3. P.J. Barnes, and M. Karin Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases N. Engl. J. Med. 336 1997 1066 1071 (Pubitemid 27163860)
4. J.B. Bederson Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats Stroke 17 1986 1304 1308 (Pubitemid 17008976)
5. E. Berdyshev Effects of cannabinoid receptor ligands on LPS-induced pulmonary inflammation in mice Life Sci. 63 1998 PL125 PL129
6. E.V. Berdyshev Stress-induced generation of N-acylethanolamines in mouse epidermal JB6 P cells Biochem J. 346 2 2000 369 374 (Pubitemid 30148122)
7. C. Berger Massive accumulation of N-acylethanolamines after stroke. Cell signalling in acute cerebral ischemia? J. Neurochem. 88 2004 1159 1167 (Pubitemid 38280683)
8. A. Blesch, and M.H. Tuszynski Cellular GDNF delivery promotes growth of motor and dorsal column sensory axons after partial and complete spinal cord transections and induces remyelination J. Comp. Neurol. 467 2003 403 417 (Pubitemid 37421083)
9. A. Bowie, and L.A. O'Neill Oxidative stress and nuclear factor-kappaB activation: a reassessment of the evidence in the light of recent discoveries Biochem. Pharmacol. 59 2000 13 23
10. P. Calabresi Ionotropic glutamate receptors: still a target for neuroprotection in brain ischemia? Insights from in vitro studies Neurobiol. Dis. 12 2003 82 88 (Pubitemid 36259970)
11. P. Calabresi Antiepileptic drugs as a possible neuroprotective strategy in brain ischemia Ann. Neurol. 53 2003 693 702 (Pubitemid 36622505)
12. A. Calignano Control of pain initiation by endogenous cannabinoids Nature 394 1998 277 281 (Pubitemid 28335039)
13. E. Candelario-Jalil, and B.L. Fiebich Cyclooxygenase inhibition in ischemic brain injury Curr. Pharm. Des. 14 2008 1401 1418 (Pubitemid 351982548)
14. E. Candelario-Jalil Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia Neuroscience 158 2009 983 994
15. M. Carlen Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke Nat. Neurosci. 12 2009 259 267
16. B. Costa The endogenous fatty acid amide, palmitoylethanolamide, has anti-allodynic and anti-hyperalgesic effects in a murine model of neuropathic pain: involvement of CB(1), TRPV1 and PPARgamma receptors and neurotrophic factors Pain 139 2008 541 550
17. B. Costa Therapeutic effect of the endogenous fatty acid amide, palmitoylethanolamide, in rat acute inflammation: inhibition of nitric oxide and cyclo-oxygenase systems Br. J. Pharmacol. 137 2002 413 420 (Pubitemid 35221894)
18. S. Cuzzocrea Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury Pharmacol. Rev. 53 2001 135 159 (Pubitemid 32173112)
19. L. De Petrocellis Palmitoylethanolamide enhances anandamide stimulation of human vanilloid VR1 receptors FEBS Lett. 506 2001 253 256 (Pubitemid 32964824)
20. M. Degn Changes in brain levels of N-acylethanolamines and 2-arachidonoylglycerol in focal cerebral ischemia in mice J. Neurochem. 103 2007 1907 1916 (Pubitemid 350126623)
21. M. Del Fiacco Topographical localization of glial cell line-derived neurotrophic factor in the human brain stem: an immunohistochemical study of prenatal, neonatal and adult brains J. Chem. Neuroanat. 23 2002 29 48 (Pubitemid 34072920)
22. W.A. Devane Determination and characterization of a cannabinoid receptor in rat brain Mol. Pharmacol. 34 1988 605 613 (Pubitemid 19007296)
23. W.A. Devane Isolation and structure of a brain constituent that binds to the cannabinoid receptor Science 258 1992 1946 1949 (Pubitemid 23026736)
24. U. Dirnagl Pathobiology of ischemic stroke: an integrated view Trends Neurosci. 22 1999 391 397 (Pubitemid 29453643)
25. H.F. Elewa Minocycline for short-term neuroprotection Pharmacotherapy 26 2006 515 521
26. Esposito Effects of palmitoylethanolamide on release of mast cell peptidases and neurotrophic factors after spinal cord injury Brain Behav. Immun. 25 2011 1099 1112
27. W.P. Farquhar-Smith, and A.S. Rice Administration of endocannabinoids prevents a referred hyperalgesia associated with inflammation of the urinary bladder Anesthesiology 94 2001 507 513 (discussion 6A) (Pubitemid 32198461)
28. J.H. Garcia Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Statistical validation Stroke 26 1995 627 634 (discussion 635)
29. P. Garg Intracellular mechanisms of N-acylethanolamine-mediated neuroprotection in a rat model of stroke Neuroscience 2010 166
30. T. Genovese Effects of palmitoylethanolamide on signaling pathways implicated in the development of spinal cord injury J. Pharmacol. Exp. Ther. 326 2008 12 23 (Pubitemid 351872139)
31. D.J. Gladstone Toward wisdom from failure: lessons from neuroprotective stroke trials and new therapeutic directions Stroke 33 2002 2123 2136 (Pubitemid 34840080)
32. J.R. Gordon, and S.J. Galli Release of both preformed and newly synthesized tumor necrosis factor alpha (TNF-alpha)/cachectin by mouse mast cells stimulated via the Fc epsilon RI. A mechanism for the sustained action of mast cell-derived TNF-alpha during IgE-dependent biological responses J. Exp. Med. 174 1991 103 107
33. Hansen Accumulation of the anandamide precursor and other N-acylethanolamine phospholipids in infant rat models of in vivo necrotic and apoptotic neuronal death J. Neurochem. 2001
34. H.H. Hansen 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 2001 39 46 (Pubitemid 32044366)
35. H.S. Hansen Glutamate stimulates the formation of N- acylphosphatidylethanolamine and N-acylethanolamine in cortical neurons in culture Biochim. Biophys. Acta 1258 1995 303 308
36. H. Hara Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage Proc. Natl. Acad. Sci. USA 94 1997 2007 2012 (Pubitemid 27113952)
37. M.S. Hussain, and A. Shuaib Research into neuroprotection must continue... But with a different approach Stroke 39 2008 521 522 (Pubitemid 351619489)
38. N. Klocker In vivo neurotrophic effects of GDNF on axotomized retinal ganglion cells Neuroreport 8 1997 3439 3442 (Pubitemid 27497460)
39. E. Kownatzki Triggering of mast cells Mol. Immunol. 19 1982 1297 1300 (Pubitemid 12021065)
40. D.M. Lambert, and V. Di Marzo The palmitoylethanolamide and oleamide enigmas: are these two fatty acid amides cannabimimetic? Curr. Med. Chem. 6 1999 757 773 (Pubitemid 29399503)
41. D.M. Lambert Anticonvulsant activity of N-palmitoylethanolamide, a putative endocannabinoid, in mice Epilepsia 42 2001 321 327 (Pubitemid 32275910)
42. D.M. Lambert The palmitoylethanolamide family: a new class of anti-inflammatory agents? Curr. Med. Chem. 9 2002 663 674 (Pubitemid 34296196)
43. A. Laurikainen Glial cell line-derived neurotrophic factor is expressed in penis of adult rat and retrogradely transported in penile parasympathetic and sensory nerves Cell Tissue Res. 302 2000 321 329
44. D. Lloyd-Jones Heart disease and stroke statistics - 2010 update: a report from the American Heart Association Circulation 121 2010 948 954
45. J. Lo Verme The nuclear receptor peroxisome proliferator-activated receptor-alpha mediates the anti-inflammatory actions of palmitoylethanolamide Mol. Pharmacol. 67 2005 15 19 (Pubitemid 40069962)
46. E.Z. Longa Reversible middle cerebral artery occlusion without craniectomy in rats Stroke 20 1989 84 91 (Pubitemid 19040218)
47. X.C. Lu Post-treatment with a novel PARG inhibitor reduces infarct in cerebral ischemia in the rat Brain Res. 978 2003 99 103
48. M. Maisel Transcription profiling of adult and fetal human neuroprogenitors identifies divergent paths to maintain the neuroprogenitor cell state Stem Cells 25 2007 1231 1240 (Pubitemid 46684883)
49. K. Mandai Ischemic damage and subsequent proliferation of oligodendrocytes in focal cerebral ischemia Neuroscience 77 1997 849 861 (Pubitemid 27100579)
50. K. Maresz Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli J. Neurochem. 95 2005 437 445 (Pubitemid 41457512)
51. L.A. Matsuda Structure of a cannabinoid receptor and functional expression of the cloned cDNA Nature 346 1990 561 564
52. M.P. Mattson Neurodegenerative disorders and ischemic brain diseases Apoptosis 6 2001 69 81 (Pubitemid 32233956)
53. S. Mazzari N-(2-hydroxyethyl)hexadecanamide is orally active in reducing edema formation and inflammatory hyperalgesia by down-modulating mast cell activation Eur. J. Pharmacol. 300 1996 227 236
54. A. Melani Selective adenosine A2a receptor antagonism reduces JNK activation in oligodendrocytes after cerebral ischaemia Brain 132 2009 1480 1495
55. A. Melani The selective A2A receptor antagonist SCH 58261 reduces striatal transmitter outflow, turning behavior and ischemic brain damage induced by permanent focal ischemia in the rat Brain Res. 959 2003 243 250 (Pubitemid 35472186)
56. A. Melani Striatal outflow of adenosine, excitatory amino acids, gamma-aminobutyric acid, and taurine in awake freely moving rats after middle cerebral artery occlusion: correlations with neurological deficit and histopathological damage Stroke 30 1999 2448 2454 (discussion 2455)
57. K. Meletis Spinal cord injury reveals multilineage differentiation of ependymal cells PLoS Biol. 6 2008 e182
58. B. Moesgaard Accumulation of N-acyl-ethanolamine phospholipids in rat brains during post-decapitative ischemia: a 31p NMR study J. Lipid Res. 40 1999 515 521 (Pubitemid 29116155)
59. 2 in endothelial cells Br. J. Pharmacol. 126 1999 1593 1600
60. H. Nakatomi Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors Cell 110 2002 429 441 (Pubitemid 35232287)
61. N.L. Parinandi, and H.H. Schmid Effects of long-chain N-acylethanolamines on lipid peroxidation in cardiac mitochondria FEBS Lett. 237 1988 49 52
62. G. Pezeshki GDNF elicits distinct immediate-early gene responses in cultured cortical and mesencephalic neurons J. Neurosci. Res. 71 2003 478 484 (Pubitemid 36158331)
63. G. Raposo Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation Mol. Biol. Cell 8 1997 2631 2645 (Pubitemid 27528227)
64. A.S. Rice Endocannabinoids and pain: spinal and peripheral analgesia in inflammation and neuropathy Prostaglandins Leukot. Essent. Fatty Acids 66 2002 243 256 (Pubitemid 34743599)
65. R.A. Ross Inhibition of nitric oxide production in RAW264.7 macrophages by cannabinoids and palmitoylethanolamide Eur. J. Pharmacol. 401 2000 121 130 (Pubitemid 30488186)
66. M. Saarma GDNF - a stranger in the TGF-beta superfamily? Eur. J. Biochem. 267 2000 6968 6971
67. H. Sariola, and M. Saarma Novel functions and signalling pathways for GDNF J. Cell Sci. 116 2003 3855 3862 (Pubitemid 37279301)
68. S.I. Savitz A critical appraisal of the NXY-059 neuroprotection studies for acute stroke: a need for more rigorous testing of neuroprotective agents in animal models of stroke Exp. Neurol. 205 2007 20 25 (Pubitemid 46621180)
69. W.R. Schabitz Synergistic effects of a combination of low-dose basic fibroblast growth factor and citicoline after temporary experimental focal ischemia Stroke 30 1999 427 431 (discussion 431-2)
70. H.H. Schmid, and E.V. Berdyshev Cannabinoid receptor-inactive N-acylethanolamines and other fatty acid amides: metabolism and function Prostaglandins Leukot. Essent. Fatty Acids 66 2002 363 376 (Pubitemid 34743609)
71. P.C. Schmid Occurrence and postmortem generation of anandamide and other long-chain N-acylethanolamines in mammalian brain FEBS Lett. 375 1995 117 120
72. M. Schomacher Endocannabinoids mediate neuroprotection after transient focal cerebral ischemia Brain Res. 1240 2008 213 220
73. J.J. Sheehan, and S.E. Tsirka Fibrin-modifying serine proteases thrombin, tPA, and plasmin in ischemic stroke: a review Glia 50 2005 340 350 (Pubitemid 40780840)
74. N.A. Shneider Gamma motor neurons express distinct genetic markers at birth and require muscle spindle-derived GDNF for postnatal survival Neural Dev. 4 2009 42
75. M.E. Sughrue Data presentation in rodent stroke studies and the predictive value of confidence intervals J. Clin. Neurosci. 17 2010 (11-5)
76. C. Szabo, and V.L. Dawson Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion Trends Pharmacol. Sci. 19 1998 287 298 (Pubitemid 28358088)
77. M. Theodosiou Hyperalgesia due to nerve damage: role of nerve growth factor Pain 81 1999 245 255 (Pubitemid 29257895)
78. F.G. Wulczyn The NF-kappa B/Rel and I kappa B gene families: mediators of immune response and inflammation J. Mol. Med. (Berlin) 74 1996 749 769 (Pubitemid 26405603)
79. J. Xu iNOS and nitrotyrosine expression after spinal cord injury J. Neurotrauma 18 2001 523 532 (Pubitemid 32472842)
80. Y. Zuo Inflammation and hyperalgesia induced by nerve injury in the rat: a key role of mast cells Pain 105 2003 467 479 (Pubitemid 37186908)