A pyrazole curcumin derivative restores membrane homeostasis disrupted after brain trauma

Experimental Neurology

Volumn 226, Issue 1, 2010, Pages 191-199

  Sharma, Sandeep ^a   Ying, Zhe ^a   Gomez Pinilla, Fernando ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

4 hydoxynonenal; Cognition; Curcumin; Membrane damage; Rat

Indexed keywords

4 HYDROXYNONENAL; CALCIUM INDEPENDENT PHOSPHOLIPASE A2; CURCUMIN DERIVATIVE; DOCOSAHEXAENOIC ACID; FATTY ACID TRANSPORTER; LIPID; LONG CHAIN FATTY ACID; MEMBRANE PHOSPHOLIPID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PYRAZOLE DERIVATIVE; SYNTAXIN; SYNTAXIN 3; UNCLASSIFIED DRUG; 4-HYDROXY-2-NONENAL; ALDEHYDE; CURCUMIN; NERVE PROTEIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG ACTIVITY; FATTY ACID TRANSPORT; HIPPOCAMPUS; LEARNING; LIPID PEROXIDATION; MALE; MEMBRANE DAMAGE; NERVE CELL PLASTICITY; NERVE FUNCTION; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC MEMBRANE; TASK PERFORMANCE; TRAUMATIC BRAIN INJURY; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; BRAIN INJURIES; COGNITION; DRUG EFFECTS; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MAZE TEST; PATHOLOGY; PSYCHOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE; WESTERN BLOTTING;

ALDEHYDES; ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN INJURIES; CELL MEMBRANE; COGNITION; CURCUMIN; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; MALE; MAZE LEARNING; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 77957764802     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.08.027     Document Type: Article

References (52)

1. Abumrad N., Coburn C., Ibrahimi A. Membrane proteins implicated in long-chain fatty acid uptake by mammalian cells: CD36, FATP and FABPm. Biochim. Biophys. Acta 1999, 1441:4-13.
2. Ansari M.A., Roberts K.N., Scheff S.W. Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury. Free Radic. Biol. Med. 2008, 45:443-452.
3. Begum A.N., Jones M.R., Lim G.P., Morihara T., Kim P., Heath D.D., Rock C.L., Pruitt M.A., Yang F., Hudspeth B., Hu S., Faull K.F., Teter B., Cole G.M., Frautschy S.A. Curcumin structure-function, bioavailability, and efficacy in models of neuroinflammation and Alzheimer's disease. J. Pharmacol. Exp. Ther. 2008, 326:196-208.
4. Biegon A. Cannabinoids as neuroprotective agents in traumatic brain injury. Curr. Pharm. Des. 2004, 10:2177-2183.
5. Calon F., Lim G.P., Morihara T., Yang F., Ubeda O., Salem N., Frautschy S.A., Cole G.M. Dietary n-3 polyunsaturated fatty acid depletion activates caspases and decreases NMDA receptors in the brain of a transgenic mouse model of Alzheimer's disease. Eur. J. Neurosci. 2005, 22:617-626.
6. Chytrova G., Ying Z., Gomez-Pinilla F. Exercise contributes to the effects of DHA dietary supplementation by acting on membrane-related synaptic systems. Brain Res. 2009.
7. Darios F., Davletov B. Omega-3 and omega-6 fatty acids stimulate cell membrane expansion by acting on syntaxin 3. Nature 2006, 440:813-817.
8. Doege H., Stahl A. Protein-mediated fatty acid uptake: novel insights from in vivo models. Physiology (Bethesda) 2006, 21:259-268.
9. Dyall S.C., Michael G.J., Whelpton R., Scott A.G., Michael-Titus A.T. Dietary enrichment with omega-3 polyunsaturated fatty acids reverses age-related decreases in the GluR2 and NR2B glutamate receptor subunits in rat forebrain. Neurobiol. Aging 2007, 28:424-439.
10. Farooqui A.A., Horrocks L.A. Phospholipase A2-generated lipid mediators in the brain: the good, the bad, and the ugly. Neuroscientist 2006, 12:245-260.
11. Farooqui A.A., Ong W.Y., Horrocks L.A. Biochemical aspects of neurodegeneration in human brain: involvement of neural membrane phospholipids and phospholipases A2. Neurochem. Res. 2004, 29:1961-1977.
12. Fitzpatrick J.S., Baudry M. Blockade of long-term depression in neonatal hippocampal slices by a phospholipase A2 inhibitor. Brain Res. Dev. Brain Res. 1994, 78:81-86.
13. Forlenza O.V., Mendes C.T., Marie S.K., Gattaz W.F. Inhibition of phospholipase A2 reduces neurite outgrowth and neuronal viability. Prostaglandins Leukot. Essent. Fatty Acids 2007, 76:47-55.
14. Gomez-Pinilla F., So V., Kesslak J.P. Spatial learning induces neurotrophin receptor and synapsin I in the hippocampus. Brain Res. 2001, 904:13-19.
15. Hashimoto M., Hossain S., Shimada T., Shido O. Docosahexaenoic acid-induced protective effect against impaired learning in amyloid beta-infused rats is associated with increased synaptosomal membrane fluidity. Clin. Exp. Pharmacol. Physiol. 2006, 33:934-939.
16. Hocquemiller M., Vitry S., Bigou S., Bruyere J., Ausseil J., Heard J.M. GAP43 overexpression and enhanced neurite outgrowth in mucopolysaccharidosis type IIIB cortical neuron cultures. J. Neurosci. Res. 2010, 88:202-213.
17. Holscher C., Canevari L., Richter-Levin G. Inhibitors of PLA2 and NO synthase cooperate in producing amnesia of a spatial task. NeuroReport 1995, 6:730-732.
18. Holscher C., Rose S.P. Inhibitors of phospholipase A2 produce amnesia for a passive avoidance task in the chick. Behav. Neural Biol. 1994, 61:225-232.
19. Kadoya A., Miyake H., Ohyashiki T. Contribution of lipid dynamics on the inhibition of bovine brain synaptosomal Na+-K+-ATPase activity induced by 4-hydroxy-2-nonenal. Biol. Pharm. Bull. 2003, 26:787-793.
20. Keller J.N., Mark R.J., Bruce A.J., Blanc E., Rothstein J.D., Uchida K., Waeg G., Mattson M.P. 4-Hydroxynonenal, an aldehydic product of membrane lipid peroxidation, impairs glutamate transport and mitochondrial function in synaptosomes. Neuroscience 1997, 80:685-696.
21. Keller J.N., Pang Z., Geddes J.W., Begley J.G., Germeyer A., Waeg G., Mattson M.P. Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid beta-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J. Neurochem. 1997, 69:273-284.
22. Lauderback C.M., Hackett J.M., Huang F.F., Keller J.N., Szweda L.I., Markesbery W.R., Butterfield D.A. The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1-42. J. Neurochem. 2001, 78:413-416.
23. Lim G.P., Chu T., Yang F., Beech W., Frautschy S.A., Cole G.M. The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J. Neurosci. 2001, 21:8370-8377.
24. Liu Y., Dargusch R., Maher P., Schubert D. A broadly neuroprotective derivative of curcumin. J. Neurochem. 2008, 105:1336-1345.
25. Liu Y., Schubert D. Steroid hormones block amyloid fibril-induced 3-(4, 5-dimethylthiazol-2-yl)-2, 5-diphenyltetrazolium bromide (MTT) formazan exocytosis: relationship to neurotoxicity. J. Neurochem. 1998, 71:2322-2329.
26. Loftis J.M., Janowsky A. The N-methyl-d-aspartate receptor subunit NR2B: localization, functional properties, regulation, and clinical implications. Pharmacol. Ther. 2003, 97:55-85.
27. Lund E.K., Harvey L.J., Ladha S., Clark D.C., Johnson I.T. Effects of dietary fish oil supplementation on the phospholipid composition and fluidity of cell membranes from human volunteers. Ann. Nutr. Metab. 1999, 43:290-300.
28. Maher P., Akaishi T., Schubert D., Abe K. A pyrazole derivative of curcumin enhances memory. Neurobiol. Aging 2008.
29. Mancuso D.J., Sims H.F., Han X., Jenkins C.M., Guan S.P., Yang K., Moon S.H., Pietka T., Abumrad N.A., Schlesinger P.H., Gross R.W. Genetic ablation of calcium-independent phospholipase A2gamma leads to alterations in mitochondrial lipid metabolism and function resulting in a deficient mitochondrial bioenergetic phenotype. J. Biol. Chem. 2007, 282:34611-34622.
30. Mark R.J., Lovell M.A., Markesbery W.R., Uchida K., Mattson M.P. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide. J. Neurochem. 1997, 68:255-264.
31. Martel M.A., Patenaude C., Menard C., Alaux S., Cummings B.S., Massicotte G. A novel role for calcium-independent phospholipase A in alpha-amino-3-hydroxy-5-methylisoxazole-propionate receptor regulation during long-term potentiation. Eur. J. Neurosci. 2006, 23:505-513.
32. McMahon H.T., Sudhof T.C. Synaptic core complex of synaptobrevin, syntaxin, and SNAP25 forms high affinity alpha-SNAP binding site. J. Biol. Chem. 1995, 270:2213-2217.
33. Merenda A., Gugliotta M., Holloway R., Levasseur J.E., Alessandri B., Sun D., Bullock M.R. Validation of brain extracellular glycerol as an indicator of cellular membrane damage due to free radical activity after traumatic brain injury. J. Neurotrauma 2008, 25:527-537.
34. Mertsch K., Blasig I., Grune T. 4-Hydroxynonenal impairs the permeability of an in vitro rat blood-brain barrier. Neurosci. Lett. 2001, 314:135-138.
35. Muller T., Albrecht D., Gebhardt C. Both NR2A and NR2B subunits of the NMDA receptor are critical for long-term potentiation and long-term depression in the lateral amygdala of horizontal slices of adult mice. Learn. Mem. 2009, 16:395-405.
36. Murakami M., Nakatani Y., Atsumi G., Inoue K., Kudo I. Regulatory functions of phospholipase A2. Crit. Rev. Immunol. 1997, 17:225-283.
37. Nakazawa K., McHugh T.J., Wilson M.A., Tonegawa S. NMDA receptors, place cells and hippocampal spatial memory. Nat. Rev. Neurosci. 2004, 5:361-372.
38. Neely M.D., Sidell K.R., Graham D.G., Montine T.J. The lipid peroxidation product 4-hydroxynonenal inhibits neurite outgrowth, disrupts neuronal microtubules, and modifies cellular tubulin. J. Neurochem. 1999, 72:2323-2333.
39. Sato T., Ishida T., Irifune M., Tanaka K., Hirate K., Nakamura N., Nishikawa T. Effect of NC-1900, an active fragment analog of arginine vasopressin, and inhibitors of arachidonic acid metabolism on performance of a passive avoidance task in mice. Eur. J. Pharmacol. 2007, 560:36-41.
40. Schaloske R.H., Dennis E.A. The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta 2006, 1761:1246-1259.
41. Sharma S., Zhuang Y., Ying Z., Wu A., Gomez-Pinilla F. Dietary curcumin supplementation counteracts reduction in levels of molecules involved in energy homeostasis after brain trauma. Neuroscience 2009, 161:1037-1044.
42. Six D.A., Dennis E.A. The expanding superfamily of phospholipase A(2) enzymes: classification and characterization. Biochim. Biophys. Acta 2000, 1488:1-19.
43. Subramaniam R., Roediger F., Jordan B., Mattson M.P., Keller J.N., Waeg G., Butterfield D.A. The lipid peroxidation product, 4-hydroxy-2-trans-nonenal, alters the conformation of cortical synaptosomal membrane proteins. J. Neurochem. 1997, 69:1161-1169.
44. Suzuki H., Park S.J., Tamura M., Ando S. Effect of the long-term feeding of dietary lipids on the learning ability, fatty acid composition of brain stem phospholipids and synaptic membrane fluidity in adult mice: a comparison of sardine oil diet with palm oil diet. Mech. Ageing Dev. 1998, 101:119-128.
45. Thiyagarajan M., Sharma S.S. Neuroprotective effect of curcumin in middle cerebral artery occlusion induced focal cerebral ischemia in rats. Life Sci. 2004, 74:969-985.
46. Wolf M.J., Izumi Y., Zorumski C.F., Gross R.W. Long-term potentiation requires activation of calcium-independent phospholipase A2. FEBS Lett. 1995, 377:358-362.
47. Wu A., Molteni R., Ying Z., Gomez-Pinilla F. A saturated-fat diet aggravates the outcome of traumatic brain injury on hippocampal plasticity and cognitive function by reducing brain-derived neurotrophic factor. Neuroscience 2003, 119:365-375.
48. Wu A., Ying Z., Gomez-Pinilla F. Dietary omega-3 fatty acids normalize BDNF levels, reduce oxidative damage, and counteract learning disability after traumatic brain injury in rats. J. Neurotrauma 2004, 21:1457-1467.
49. Wu A., Ying Z., Gomez-Pinilla F. The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. Eur. J. Neurosci. 2004, 19:1699-1707.
50. Wu A., Ying Z., Gomez-Pinilla F. Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress, synaptic plasticity, and cognition. Exp. Neurol. 2006, 197:309-317.
51. Yang F., Lim G.P., Begum A.N., Ubeda O.J., Simmons M.R., Ambegaokar S.S., Chen P.P., Kayed R., Glabe C.G., Frautschy S.A., Cole G.M. Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J. Biol. Chem. 2005, 280:5892-5901.
52. Zhao J., Zhao Y., Zheng W., Lu Y., Feng G., Yu S. Neuroprotective effect of curcumin on transient focal cerebral ischemia in rats. Brain Res. 2008, 1229:224-232.