Olfactory discrimination ability and brain expression of c-fos, Gir and Glut1 mRNA are altered in n - 3 fatty acid-depleted rats

Behavioural Brain Research

Volumn 184, Issue 1, 2007, Pages 1-10

  Hichami, Aziz ^a   Datiche, Frédérique ^b   Ullah, Sana ^a   Liénard, Fabienne ^b   Chardigny, Jean Michel ^c   Cattarelli, Martine ^d,e   Khan, Naim Akhtar ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

^c CRNH AUVERGNE   (France)

^d UNIVERSITÉ DE LYON   (France)

^e UNIVERSITÉ LYON 1   (France)

Author keywords

Brain; c fos; Docosahexaenoic acid; Gir; Glut1; n 3 deficiency; Olfactory learning; Rat

Indexed keywords

DOCOSAHEXAENOIC ACID; GLUCOSE TRANSPORTER 1; MESSENGER RNA; OMEGA 3 FATTY ACID; POLYUNSATURATED FATTY ACID; PROTEIN; PROTEIN C FOS; PROTEIN GIR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; FAT INTAKE; LEARNING; MALE; MAZE TEST; NEOCORTEX; NEUROCHEMISTRY; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PYRIFORM CORTEX; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN; DIET, FAT-RESTRICTED; DISCRIMINATION (PSYCHOLOGY); DISCRIMINATION LEARNING; FATTY ACIDS, OMEGA-3; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORTER TYPE 1; MALE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SMELL; TIME FACTORS;

EID: 34548616866     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2007.06.010     Document Type: Article

References (57)

1. Abraham W.C., Mason S.E., Demmer J., Williams J.M., Richardson C.L., Tate W.P., et al. Correlations between immediate early gene induction and the persistence of long-term potentiation. Neuroscience 56 (1993) 717-727
2. Alessandri J.M., Guesnet P., Vancassel S., Astorg P., Denis I., Langelier B., et al. Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life. Reprod Nutr Dev 44 (2004) 509-538
3. Bertaina-Anglade V., Tramu G., and Destrade C. Differential learning-stage dependent patterns of c-fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice. Eur J Neurosci 12 (2000) 3803-3812
4. Blight E.G., and Dyer W.J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37 (1959) 911-917
5. Bourre J.M., Francois M., Youyou A., Dumont O., Piciotti M., Pascal G., et al. The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J Nutr 119 (1989) 1880-1892
6. Calderon F., and Kim H.Y. Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J Neurochem 90 (2004) 979-988
7. Catalan J., Moriguchi T., Slotnick B., Murthy M., Greiner R.S., and Salem Jr. N. Cognitive deficits in docosahexaenoic acid-deficient rats. Behav Neurosci 116 (2002) 1022-1031
8. Choeiri C., Staines W., Miki T., Seino S., and Messier C. Glucose transporter plasticity during memory processing. Neuroscience 130 (2005) 591-600
9. Dalley J.W., Cardinal R.N., and Robbins T.W. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28 (2004) 771-784
10. Delion S., Chalon S., Guilloteau D., Besnard J.C., and Durand G. Alpha-Linolenic acid dietary deficiency alters age-related changes of dopaminergic and serotoninergic neurotransmission in the rat frontal cortex. J. Neurochem 66 (1996) 1582-1591
11. Denys A., Hichami A., Maume B., and Khan N.A. Docosahexaenoic acid modulates phorbol ester-induced activation of extracellular signal-regulated kinases 1 and 2 in NIH/3T3 cells. Lipids 36 (2001) 813-818
12. Favrelere S., Stadelmann-Ingrand S., Huguet F., De Javel D., Piriou A., Tallineau C., et al. Age-related changes in ethanolamine glycerophospholipid fatty acid levels in rat frontal cortex and hippocampus. Neurobiol Aging 21 (2000) 653-660
13. Fujita S., Ikegaya Y., Nishikawa M., Nishiyama N., and Matsuki N. Docosahexaenoic acid improves long-term potentiation attenuated by phospholipase A(2) inhibitor in rat hippocampal slices. Br J Pharmacol (2001) 17-22
14. Gamoh S., Hashimoto M., Hossain S., and Masumura S. Chronic administration of docosahexaenoic acid improves the performance of radial arm maze task in aged rats. Clin Exp Pharmacol Physiol 28 (2001) 266-270
15. Gerbi A., Zerouga M., Debray M., Durand G., Chanez C., and Bourre J.M. Effect of fish oil diet on fatty acid composition of phospholipids of brain membranes and on kinetic properties of Na+, K(+)-ATPase isoenzymes of weaned and adult rats. J Neurochem 62 (1994) 1560-1569
16. Greiner R.S., Moriguchi T., Hutton A., Slotnick B.M., and Salem Jr. N. Rats with low levels of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks. Lipids 34 (1999) S239-S243
17. Greiner R.S., Moriguchi T., Slotnick B.M., Hutton A., and Salem Jr. N. Olfactory discrimination deficits in n - 3 fatty acid-deficient rats. Physiol Behav 72 (2001) 379-385
18. Herrera D.G., and Robertson H.A. Activation of c-fos in the brain. Prog Neurobiol 50 (1996) 83-107
19. Hussain S.T., and Roots B.I. Effect of essential fatty acid deficiency & immunopathological stresses on blood brain barrier (B-BB) in Lewis rats: a biochemical study. Biochem Soc Trans 22 (1994) 338S
20. Ikemoto A., Nitta A., Furukawa S., Ohishi M., Nakamura A., Fujii Y., et al. Dietary n - 3 fatty acid deficiency decreases nerve growth factor content in rat hippocampus. Neurosci Lett 285 (2000) 99-102
21. Kaczmarek L. Gene expression in learning processes. Acta Neurobiol Exp 60 (2000) 419-424
22. Khan N.A., Yessoufou A., Kim M., and Hichami A. n - 3 fatty acids modulate Th1 and Th2 dichotomy in diabetic pregnancy and macrosomia. J Autoimmun 26 (2006) 268-277
23. Kim H.Y., and Edsall L. The role of docosahexaenoic acid (22:6n - 3) in neuronal signaling. Lipids 34 Suppl (1999) S249-S250
24. Kim H.Y., Akbar M., Lau A., and Edsall L. Inhibition of neuronal apoptosis by docosahexaenoic acid (22:6n - 3). Role of phosphatidylserine in antiapoptotic effect. J Biol Chem 275 (2000) 35215-35223
25. Lefkowitz W., Lim S.Y., Lin Y., and Salem Jr. N. Where does the developing brain obtain its docosahexaenoic acid? Relative contributions of dietary alpha-linolenic acid, docosahexaenoic acid, and body stores in the developing rat. Pediatr Res 57 (2005) 157-165
26. Lim S., and Suzuki H. Changes in maze behavior of mice occur after sufficient accumulation of docosahexaenoic acid in brain. J Nutr 131 (2001) 319-324
27. Lim S.Y., Doherty J.D., McBride K., Miller-Ihli N.J., Carmona G.N., Stark K.D., et al. Lead exposure and (n - 3) fatty acid deficiency during rat neonatal development affect subsequent spatial task performance and olfactory discrimination. J Nutr 135 (2005) 1019-1026
28. Litaudon P., Mouly A.M., Sullivan R., Gervais R., and Cattarelli M. Learning-induced changes in rat piriform cortex activity mapped using multisite recording with voltage sensitive dye. Eur J Neurosci 9 (1997) 1593-1602
29. Madani S., Hichami A., Legrand A., Belleville J., and Khan N.A. Implication of acyl chain of diacylglycerols in activation of different isoforms of protein kinase C. FASEB J 15 (2001) 2595-2601
30. Madani S., Hichami A., Cherkaoui-Malki M., and Khan N.A. Diacylglycerols containing Omega 3 and Omega 6 fatty acids bind to RasGRP and modulate MAP kinase activation. J Biol Chem 279 (2004) 1176-1183
31. Moriguchi T., Greiner R.S., and Salem Jr. N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J. Neurochem 75 (2000) 2563-2573
32. Moriguchi T., and Salem Jr. N. Recovery of brain docosahexaenoate leads to recovery of spatial task performance. J Neurochem 87 (2003) 297-309
33. Mouly A.M., Kindermann U., Gervais R., and Holley A. Involvement of the olfactory bulb in consolidation processes associated with long-term memory in rats. Behav Neurosci 107 (1993) 451-457
34. Neuringer M., Connor W.E., Lin D.S., Barstad L., and Luck S. Biochemical and functional effects of prenatal and postnatal omega 3 fatty acid deficiency on retina and brain in rhesus monkeys. Proc Natl Acad Sci. USA 83 (1986) 4021-4025
35. Niu S.L., Mitchell D.C., and Litman B.J. Optimization of receptor-G protein coupling by bilayer lipid composition II: formation of metarhodopsin II-transducin complex. J Biol Chem 276 (2001) 42807-42811
36. Nishikawa M., Kimura S., and Akaike N. Facilitatory effect of docosahexaenoic acid on N-methyl-d-aspartate response in pyramidal neurones of rat cerebral cortex. J Physiol 475 (1994) 83-93
37. Oguzhan B., Zhang Y., Louchami K., Courtois P., Portois L., Chardigny J.-M., et al. Pancreatic islet function in ω3 fatty acid-depleted rats. Glucose metabolism and nutrient-stimulated insulin release. Endocrine 29 (2006) 467-476
38. Roullet F., Datiche F., Liénard F., and Cattarelli M. Learning-stage dependent Fos expression in the rat brain during acquisition of an olfactory discrimination task. Behav Brain Res 157 (2005) 127-137
39. Roullet F., Liénard F., Datiche F., and Cattarelli M. Fos protein expression in olfactory-related brain areas after learning and after reactivation of a slowly acquired olfactory task in the rat. Learn Mem 12 (2005) 307-317
40. Saar D., Grossman Y., and Barkai E. Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur J Neurosci 10 (1998) 1518-1523
41. Sah R., Pritchard L.M., Richtand N.M., Ahlbrand R.L., Eaton K., Sallee F.R., et al. Expression of the glucocorticoid-induced receptor mRNA in rat brain. Neuroscience 133 (2005) 281-292
42. Salcedo E., Zhang C., Kronberg E., and Restrepo D. Analysis of training-induced changes in ethyl acetate odor maps using a new computational tool to map the glomerular layer of the olfactory bulb. Chem Senses 30 (2005) 615-626
43. Salem Jr. N., Kim H.Y., and Yergey J.A. Docosahexaenoic acid: membrane function and metabolism. In: Simopoulos A.P., Kifer R.R., and Martin R. (Eds). Health effects of polyunsaturated fatty acids in seafoods (1986), Academic Press, New York 263-317
44. Salem Jr. N., Moriguchi T., Greiner R.S., McBride K., Ahmad A., Catalan J.N., et al. Alterations in brain function after loss of docosahexaenoate due to dietary restriction of n - 3 fatty acids. J Mol Neurosci 16 (2001) 299-307
45. Slotnick B. Animal cognition and the rat olfactory system. TICS 5 (2001) 216-222
46. Slotnick B., and Bodyak N. Odor discrimination and odor quality perception in rats with disruption of connections between the olfactory epithelium and olfactory bulbs. J Neurosci 22 (2002) 4205-4216
47. Soderberg M., Edlund C., Kristensson K., and Dallner G. Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids 26 (1991) 421-425
48. Takeuchi T., Fukumoto Y., and Harada E. Influence of a dietary n - 3 fatty acid deficiency on the cerebral catecholamine contents, EEG and learning ability in rat. Behav Brain Res 131 (2002) 193-203
49. Tanabe Y., Hashimoto M., Sugioka K., Maruyama M., Fujii Y., Hagiwara R., et al. Improvement of spatial cognition with dietary docosahexaenoic acid is associated with an increase in Fos expression in rat CA1 hipPCxampus. Clin Exp Pharmacol Physiol 31 (2004) 700-703
50. Triboulot C., Hichami A., Denys A., and Khan N.A. Dietary (n - 3) polyunsaturated fatty acids exert antihypertensive effects by modulating calcium signaling in T cells of rats. J Nutr 131 (2001) 2364-2369
51. Tronel S., and Sara S.J. Mapping of olfactory memory circuits: region-specific c-fos activation after odor-reward associative learning or after its retrieval. Learn Mem 9 (2002) 105-111
52. Vreugdenhil M., Bruehl C., Voskuyl R.A., Kang J.X., Leaf A., and Wadman W.J. Saturated fatty acids modulate sodium and calcium currents in CA1 neurons. Proc Natl Acad Sci USA 93 (1996) 12559-12563
53. Wainwright P.E., Huang Y.S., Coscina D.V., Levesque S., and McCutcheon D. Brain and behavioral effects of dietary n - 3 deficiency in mice: a three generational study. Dev Psychobiol 27 (1994) 467-487
54. Wang D., Herman J.P., Pritchard L.M., Spitzer R.H., Ahlbrand R.L., Kramer G.L., et al. Cloning, expression and regulation of a glucocorticoid-induced receptor in rat brain: effect of repetitive amphetamine. J Neurosci 21 (2001) 9027-9035
55. Ximenes da Silva A., Lavialle F., Gendrot G., Guesnet P., Alessandri J.M., and Lavialle M. Glucose transport and utilization are altered in the brain of rats deficient in n - 3 polyunsaturated fatty acids. J Neurochem 81 (2002) 1328-1337
56. Yamamoto N., Saitoh M., Moriuchi A., Nomura M., and Okuyama H. Effect of dietary alphalinolenate/linoleate balance on brain lipid compositions and learning ability of rats. J Lipid Res 28 (1987) 144-151
57. Yougentob S.L., Schwob J.E., Sheehe P.R., and Yougentob L.M. Odorant threshold following methyl bromide-induced lesions of the olfactory epithelium. Physiol Behav 62 (1997) 1241-1252