Behavioral and neurochemical effects of dietary methyl donor deficiency combined with unpredictable chronic mild stress in rats

Behavioural Brain Research

Volumn 261, Issue , 2013, Pages 8-16

  Javelot, H ^a,b,c   Messaoudi, M ^b   Jacquelin, C ^a   Bisson, J F ^b   Rozan, P ^b   Nejdi, A ^b   Lazarus, C ^d   Cassel, J C ^d   Strazielle, C ^a,e   Lalonde, R ^f  

^a UNIVERSITÉ DE LORRAINE   (France)

^b ETAP Applied Ethology   (France)

^c Clinical Pharmacy Service Mental Health Establishment (EPSAN)   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e UNIVERSITÉ DE LORRAINE   (France)

^f UNIVERSITÉ DE ROUEN   (France)

Author keywords

B vitamin; Behavior; Chronic mild stress; Depression; Methyl donors; Rat

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; CORTICOSTERONE; DOPAMINE; HOMOCYSTEINE; METHYL GROUP; SEROTONIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BRAIN REGION; CHRONIC STRESS; CONTROLLED STUDY; CORPUS STRIATUM; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DIET RESTRICTION; DOPAMINE BRAIN LEVEL; ELEVATED PLUS MAZE TEST; ENVIRONMENTAL STRESS; FORCED SWIM TEST; HYPERHOMOCYSTEINEMIA; HYPOTHALAMUS; INFANT; LOCOMOTION; NEUROCHEMISTRY; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; RAT; SENSORIMOTOR CORTEX; SEROTONIN BRAIN LEVEL;

B-VITAMIN; BEHAVIOR; CHRONIC MILD STRESS; DEPRESSION; METHYL DONORS; RAT;

ANALYSIS OF VARIANCE; ANIMALS; BIOGENIC AMINES; BRAIN; CHOLINE DEFICIENCY; CHRONIC DISEASE; CORTICOSTERONE; DIET; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FOLIC ACID DEFICIENCY; HOMOCYSTEINE; MAZE LEARNING; RATS; RATS, WISTAR; SPINAL CORD; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 84890828160     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.11.047     Document Type: Article

References (70)

1. Frankenburg F.R. The role of one-carbon metabolism in schizophrenia and depression. Harv Rev Psychiatry 2007, 15(4):146-160.
2. Kronenberg G., Colla M., Endres M. Folic acid, neurodegenerative and neuropsychiatric disease. Curr Mol Med 2009, 9(3):315-323.
3. Hutto B.R. Folate and cobalamin in psychiatric illness. Compr Psychiatry 1997, 38(6):305-314.
4. Stahl S.M. Novel therapeutics for depression: l-methylfolate as a trimonoamine modulator and antidepressant-augmenting agent. CNS Spectr 2007, 12(10):739-744.
5. Miller A.L. The methylation, neurotransmitter, and antioxidant connections between folate and depression. Altern Med Rev 2008, 13(3):216-226.
6. Gilbody S., Lewis S., Lightfoot T. Methylenetetrahydrofolatereductase (MTHFR) genetic polymorphisms and psychiatric disorders: a HuGE review. Am J Epidemiol 2007, 165:1-13.
7. Guaraldi G.P., Fava M., Mazzi F., la Greca P. An open trial of methyltetrahydrofolate in elderly depressed patients. Ann Clin Psychiatry 1993, 5:101-105.
8. Kagan B.L., Sultzer D.L., Rosenlicht N., Gerner R.H. Oral S-adenosylmethionine in depression: a randomized, double-blind, placebo-controlled trial. Am J Psychiatry 1990, 147:591-595.
9. Coppen A., Bailey J. Enhancement of the antidepressant action of fluoxetine by folic acid: a randomised, placebo controlled trial. J Affect Disord 2000, 60:121-130.
10. Alpert J.E., Mischoulon D., Rubenstein G.E., Bottonari K., Nierenberg A.A., Fava M. Folinic acid (Leucovorin) as an adjunctive treatment for SSRI-refractory depression. Ann Clin Psychiatry 2002, 14(1):33-38.
11. Czyrak A., Rogóz Z., Skuza G., Zajaczkowski W., Maj J. Antidepressant activity of S-adenosyl-l-methionine in mice and rats. J Basic Clin Physiol Pharmacol 1992, 3(1):1-17.
12. Benelli A., Filaferro M., Bertolini A., Genedani S. Influence of S-adenosyl-l-methionine on chronic mild stress-induced anhedonia in castrated rats. Br J Pharmacol 1999, 127(3):645-654.
13. Genedani S., Saltini S., Benelli A., Filaferro M., Bertolini A. Influence of SAMe on the modifications of brain polyamine levels in an animal model of depression. Neuroreport 2001, 12(18):3939-3942.
14. Molina-Hernández M., Téllez-Alcántara N.P. Fluoxetine, 17-β estradiol or folic acid combined with intra-lateral septal infusions of neuropeptide Y produced antidepressant-like actions in ovariectomized rats forced to swim. Peptides 2011, 32(12):2400-2406.
15. Molina-Hernández M., Téllez-Alcántara N.P., Olivera-López J.I., Jaramillo M.T. The folic acid combined with 17-β estradiol produces antidepressant-like actions in ovariectomized rats forced to swim. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35(January (1)):60-66.
16. Brocardo P.S., Budni J., Lobato K.R., Santos A.R., Rodrigues A.L. Evidence for the involvement of the opioid system in the antidepressant-like effect of folic acid in the mouse forced swimming test. Behav Brain Res 2009, 200(1):122-127.
17. Brocardo P.S., Budni J., Lobato K.R., Kaster M.P., Rodrigues A.L. Antidepressant-like effect of folic acid: involvement of NMDA receptors and l-arginine-nitric oxide-cyclic guanosine monophosphate pathway. Eur J Pharmacol 2008, 598(1-3):37-42.
18. Brocardo P.S., Budni J., Kaster M.P., Santos A.R., Rodrigues A.L. Folic acid administration produces an antidepressant-like effect in mice: evidence for the involvement of the serotonergic and noradrenergic systems. Neuropharmacology 2008, 54(2):464-473.
19. Lalonde R., Barraud H., Ravey J., Guéant J.L., Bronowicki J.P., Strazielle C. Effects of a B-vitamin-deficient diet on exploratory activity, motor coordination, and spatial learning in young adult Balb/c mice. Brain Res 2008, 1188:122-131.
20. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005, 52(2):90-110.
21. Fraguas R., Papakostas G.I., Mischoulon D., Bottiglieri T., Alpert J., Fava M. Anger attacks in major depressive disorder and serum levels of homocysteine. Biol Psychiatry 2006, 60(3):270-274.
22. Mineur Y.S., Prasol D.J., Belzung C., Crusio W.E. Agonistic behavior and unpredictable chronic mild stress in mice. Behav Genet 2003, 33(5):513-519.
23. Blaise S.A., Nédélec E., Schroeder H., Alberto J.M., Bossenmeyer-Pourié C., Guéant J.L., et al. Gestational vitamin B deficiency leads to homocysteine-associated brain apoptosis and alters neurobehavioral development in rats. Am J Pathol 2007, 170(2):667-679.
24. Pellow S., Chopin P., File S.E., Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985, 14:149-167.
25. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 1985, 9(1):37-44.
26. Porsolt R.D., Epichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
27. Amouzou E.K., Chabi N.W., Adjalla C.E., Rodriguez-Guéant R.M., Feillet F., Villaume C., et al. High prevalence of hyperhomocysteinemia related to folate deficiency and the 677C→T mutation of the gene encoding methylenetetrahydrofolate reductase in coastal West Africa. Am J Clin Nutr 2004, 79(4):619-624.
28. Bats S., Thoumas J.L., Lordi B., Tonon M.C., Lalonde R., Caston J. The effects of a mild stressor on spontaneous alternation in mice. Behav Brain Res 2001, 118(1):11-15.
29. Durand P., Prost M., Blache D. Folic acid deficiency enhances oral contraceptive-induced platelet hyperactivity. Arterioscler Thromb Vasc Biol 1997, 17(10):1939-1946.
30. Nieman K.M., Hartz C.S., Szegedi S.S., Garrow T.A., Sparks J.D., Schalinske K.L. Folate status modulates the induction of hepatic glycine N-methyltransferase and homocysteine metabolism in diabetic rats. Am J Physiol Endocrinol Metab 2006, 291(6):E1235-E1242.
31. Kim J.M., Lee H., Chang N. Hyperhomocysteinemia due to short-term folate deprivation is related to electron microscopic changes in the rat brain. J Nutr 2002, 132(11):3418-3421.
32. Ebbesen L.S., Ingerslev J. Folate deficiency-induced hyperhomocysteinemia attenuates, and folic acid supplementation restores, the functional activities of rat coagulation factors XII, X, and II. J Nutr 2005, 135(8):1836-1840.
33. Bielajew C., Konkle A.T., Merali Z. The effects of chronic mild stress on male Sprague-Dawley and Long Evans rats: I. Biochemical and physiological analyses. Behav Brain Res 2002, 136(2):583-592.
34. Grippo A.J., Francis J., Beltz T.G., Felder R.B., Johnson A.K. Neuroendocrine and cytokine profile of chronic mild stress-induced anhedonia. Physiol Behav 2005, 84(5):697-706.
35. Cascalheira J.F., Parreira M.C., Viegas A.N., Faria M.C., Domingues F.C. Serum homocysteine: relationship with circulating levels of cortisol and ascorbate. Ann Nutr Metab 2008, 53(1):67-74.
36. Terzidis K., Panoutsopoulos A., Mantzou A., Tourli P., Papageorgiou G., Saltiki K., et al. Cortisol levels and metabolic parameters in middle- and advanced-age subjects: associations with age. J Endocrinol Invest 2011, 34(11):e398-e402.
37. Berg A.L., Rafnsson A.T., Johannsson M., Hultberg B., Arnadottir M. The effects of adrenocorticotrophic hormone and cortisol on homocysteine and vitamin B concentrations. Clin Chem Lab Med 2006, 44(5):628-631.
38. Li L.F., Lu J., Li X.M., Xu C.L., Yang J., Qu R., et al. Antidepressant-like effects of the saponins extracted from Chaihu-jia-longgu-muli-tang in a rat unpredictable chronic mild stress model. Fitoterapia 2012, 83(1):93-103.
39. Li Y., Zheng X., Liang J., Peng Y. Coexistence of anhedonia and anxiety-independent increased novelty-seeking behavior in the chronic mild stress model of depression. Behav Processes 2010, 83(3):331-339.
40. Lalonde R., Strazielle C. Relations between open-field, elevated plus-maze, and emergence tests as displayed by C57BL/6J and BALB/c mice. J Neurosci Methods 2008, 171:48-52.
41. Routtenberg A., Kuznesof A.W. Self-starvation of rats living in activity wheels on a restricted feeding schedule. J Comp Physiol Psychol 1967, 64(3):414-421.
42. Görisch J., Schwarting R.K. Wistar rats with high versus low rear activity differ in radial maze performance. Neurobiol Learn Mem 2006, 86:175-187.
43. Inoue K., Zorrilla E.P., Tabarin A., Valdez G.R., Iwasaki S., Kiriike N., et al. Reduction of anxiety after restricted feeding in the rat: implication for eating disorders. Biol Psychiatry 2004, 55(11):1075-1081.
44. Myers B., Greenwood-Van Meerveld B. Elevated corticosterone in the amygdala leads to persistent increases in anxiety-like behavior and pain sensitivity. Behav Brain Res 2010, 214:465-469.
45. Alcaro A., Cabib S., Ventura R., Puglisi-Allegra S. Genotype- and experience-dependent susceptibility to depressive-like responses in the forced-swimming test. Psychopharmacology (Berl) 2002, 164(2):138-143.
46. Miguel T.L., Pobbe R.L., Spiacci A., Zangrossi H. Dorsal raphe nucleus regulation of a panic-like defensive behavior evoked by chemical stimulation of the rat dorsal periaqueductal gray matter. Behav Brain Res 2010, 213(2):195-200.
47. Broocks A., Liu J., Pirke K.M. Semistarvation-induced hyperactivity compensates for decreased norepinephrine and dopamine turnover in the mediobasal hypothalamus of the rat. J Neural Transm Gen Sect 1990, 79(1-2):113-124.
48. Jezová D., Jurcovicová J., Vigas M., Murgas K., Labrie F. Increase in plasma ACTH after dopaminergic stimulation in rats. Psychopharmacology 1985, 85:201-203.
49. Patrick L.R. Restless legs syndrome: pathophysiology and the role of iron and folate. Altern Med Rev 2007, 12(2):101-112.
50. Ziemińska E., Stafiej A., Łazarewicz J.W. Role of group I metabotropic glutamate receptors and NMDA receptors in homocysteine-evoked acute neurodegeneration of cultured cerebellar granule neurons. Neurochem Int 2003, 43(4-5):481-492.
51. Lipton S.A., Kim W.K., Choi Y.B., Kumar S., D'Emilia D.M., Rayudu P.V., et al. Neurotoxicity associated with dual actions of homocysteine at the N-methyl-d-aspartate receptor. Proc Natl Acad Sci U S A 1997, 94(11):5923-5928.
52. Jara-Prado A., Ortega-Vazquez A., Martinez-Ruano L., Rios C., Santamaria A. Homocysteine-induced brain lipid peroxidation: effects of NMDA receptor blockade, antioxidant treatment, and nitric oxide synthase inhibition. Neurotox Res 2003, 5(4):237-243.
53. Vieira C., De Lima T.C., Carobrez Ade P., Lino-de-Oliveira C. Frequency of climbing behavior as a predictor of altered motor activity in rat forced swimming test. Neurosci Lett 2008, 445(2):170-173.
54. Bekris S., Antoniou K., Daskas S., Papadopoulou-Daifoti Z. Behavioural and neurochemical effects induced by chronic mild stress applied to two different rat strains. Behav Brain Res 2005, 161(1):45-59.
55. Ashcroft G.W., Sharman D.F. 5-Hydroxyindoles in human cerebrospinal fluids. Nature 1960, 186:1050-1051.
56. Botez M.I., Young S.N., Bachevalier J., Gauthier S. Folate deficiency and decreased brain 5-hydroxytryptamine synthesis in man and rat. Nature 1979, 278:182-183.
57. Botez M.I., Young S.N., Bachevalier J., Gauthier S. Effect of folic acid and vitamin B12 deficiencies on 5-hydroxyindoleacetic acid in human cerebrospinal fluid. Ann Neurol 1982, 12:479-484.
58. Biegon A. Effects of steroid hormones on the serotonergic system. Ann N Y Acad Sci 1990, 600:427-434.
59. Morgan W.W., Rudeen P.K., Pfeil K.A. Effect of immobilization stress on serotonin content and turnover in regions of the rat brain. Life Sci 1975, 17(1):143-150.
60. Adell A., Garcia-Marquez C., Armario A., Gelpi E. Chronic stress increases serotonin and noradrenaline in rat brain and sensitizes their responses to a further acute stress. J Neurochem 1988, 50(6):1678-1681.
61. Petty F., Kramer G., Larrison A. Neurochemistry of stress: regional brain levels of biogenic amines and metabolites with ten different stressors. Biogen Amines 1996, 12:377-394.
62. Blanc S., Somody L., Gharib A., Gauquelin G., Gharib C., Sarda N. Counteraction of spaceflight-induced changes in the rat central serotonergic system by adrenalectomy and corticosteroid replacement. Neurochem Int 1998, 33(4):375-382.
63. Yi L.T., Li J.M., Li Y.C., Pan Y., Xu Q., Kong L.D. Antidepressant-like behavioral and neurochemical effects of the citrus-associated chemical apigenin. Life Sci 2008, 82(13-14):741-751.
64. Ahmad A., Rasheed N., Banu N., Palit G. Alterations in monoamine levels and oxidative systems in frontal cortex, striatum, and hippocampus of the rat brain during chronic unpredictable stress. Stress 2010, 13(4):355-364.
65. Koukopoulos A., Koukopoulos A. Agitated depression as a mixed state and the problem of melancholia. Psychiatr Clin North Am 1999, 22(3):547-564.
66. Fava M., Borus J.S., Alpert J.E., Nierenberg A.A., Rosenbaum J.F., Bottiglieri T. Folate, vitamin B12, and homocysteine in major depressive disorder. Am J Psychiatry 1997, 154(3):426-428.
67. Gold P.W., Chrousos G.P. The endocrinology of melancholic and atypical depression: relation to neurocircuitry and somatic consequences. Proc Assoc Am Physicians 1999, 111(1):22-34.
68. Alexopoulos G.S., Vrontou C., Kakuma T., Meyers B.S., Young R.C., Klausner E., et al. Disability in geriatric depression. Am J Psychiatry. 1996, 153(7):877-885.
69. Dimopoulos N., Piperi C., Salonicioti A., Psarra V., Gazi F., Papadimitriou A., et al. Correlation of folate, vitamin B12 and homocysteine plasma levels with depression in an elderly Greek population. Clin Biochem 2007, 40(9-10):604-608.
70. Kim J.M., Stewart R., Kim S.W., Yang S.J., Shin I.S., Yoon J.S. Predictive value of folate, vitamin B12 and homocysteine levels in late-life depression. Br J Psychiatry 2008, 192(4):268-274.