Maternal deprivation induces depressive-like behaviour and alters neurotrophin levels in the rat brain

Neurochemical Research

Volumn 36, Issue 3, 2011, Pages 460-466

  Réus, Gislaine Z ^a   Stringari, Roberto B ^a   Ribeiro, Karine F ^a   Cipriano, Andreza L ^a   Panizzutti, Bruna S ^b   Stertz, Laura ^b   Lersch, Camila ^b   Kapczinski, Flávio ^b   Quevedo, João ^a  

^a UNIVERSIDADE DO EXTREMO SUL CATARINENSE   (Brazil)

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

Author keywords

Brain derived neurotrophic factor; Depression; Maternal deprivation; Nerve growth factor; Neurotrophin 3

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOTROPIN; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3;

ADULT ANIMAL; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN TISSUE; CLIMBING; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; DEPRESSION; FEMALE; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMOBILIZATION; LOCOMOTION; MALE; MATERNAL DEPRIVATION; NONHUMAN; OPEN FIELD TEST; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT;

ANIMALS; BRAIN; CHILD; DEPRESSION; FEMALE; HUMANS; MALE; MATERNAL DEPRIVATION; NERVE GROWTH FACTORS; NEUROPSYCHOLOGICAL TESTS; PREGNANCY; RATS; RATS, WISTAR; SWIMMING;

RATTUS;

EID: 79954418775     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-010-0364-3     Document Type: Article

References (57)

1. Agid O, Shapira B, Zislin J, Ritsner M, Hanin B, Murad H, Troudart T, Bloch M, Heresco-Levy U, Lerer B (1999) Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Mol Psychiatry 4:163-172. (Pubitemid 29163979)
2. Tandberg E, Larsen JP, Aarsland D, Cummings JL (1996) The occurrence of depression in Parkinson's disease. A communitybased study. Arch Neurol 53:175-179. (Pubitemid 26055265)
3. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM (2002) Neurobiology of depression. Neuron 34:13-25. (Pubitemid 34270695)
4. Martinowich K, Manji H, Lu B (2007) New insights into BDNF function in depression and anxiety. Nat Neurosci 10:1089-1093. (Pubitemid 47339961)
5. Garcia LB, Comim CM, Valvassori SS, Réus GZ, Barbosa LM, Andreazza AC, Stertz L, Fries G, Gavioli E, Kapczinski F, Quevedo J (2008) Acute administration of ketamine induces antidepressant-like effects in the forced swimming test and increases BDNF levels in the rat hippocampus. Prog-Neuropsychopharmacol Biol Psychiatry 32:140-144.
6. Garcia LB, Comim CM, Valvassori SS, Réus GZ, Barbosa LM, Andreazza AC, Stertz L, Fries G, Gavioli E, Kapczinski F, Quevedo J (2008) Chronic administration of ketamine elicits antidepressant-like effects in rats without affecting hippocampal brain-derived neurotrophic factor protein levels. Basic Clin Pharmacol Toxicol 103:502-506.
7. Garcia LSB, Comim CM, Valvassori SS, Réus GZ, Stertz L, Kapczinski F, Gavioli EC, Quevedo J (2009) Ketamine treatment reverses behavioral and physiological alterations induced by chronic mild stress in rats. Prog Neuropsychopharmacol Biol Psychiatry 30:450-455.
8. Krishnan V, Nestler EJ (2008) The molecular neurobiology of depression. Nature 455:894-902.
9. Matthews K, Robbins TW (2003) Early experience as a determinant of adult behavioural responses to reward: the effects of repeated maternal separation in the rat. Neurosci Biobehav Rev 27: 45-55. (Pubitemid 36535389)
10. Kosten TA, Lee HJ, Kim JJ (2007) Neonatal handling alters learning in adult male and female rats in a task-specific manner. Brain Res 18:144-153. (Pubitemid 46856337)
11. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24:677-736. (Pubitemid 32695243)
12. Fortunato JJ, Réus GZ, Kirsch TM, Stringari RB, Stertz L, Kapczinski F, Pinto JP, Hallak JE, Zuardi AW, Crippa JA, Quevedo J (2009) Acute harmine administration induces antidepressant- like effects and increases BDNF levels in the rat hippocampus. Prog Neuropsychopharmacol Biol Psychiatry 33: 1425-1430.
13. Trajkovska V, Santini MA, Marcussen AB, Thomsen MS, Hansen HH, Mikkelsen JD, Arneberg L, Kokaia M, Knudsen GM, Aznar S (2009) BDNF downregulates 5-HT2A receptor protein levels in hippocampal cultures. Neurochem Int 55:697-702.
14. Cirulli F, Micera A, Alleva E, Aloe L (1998) Early maternal separation increases NGF expression in the developing rat hippocampus. Pharmacol Biochem Behav 59:853-858. (Pubitemid 28237896)
15. Faure J, Uys JD, Marais L, Stein DJ, Daniels WM (2006) Early maternal separation followed by later stressors leads to dysregulation of the HPA-axis and increases in hippocampal NGF and NT-3 levels in a rat model. Metab Brain Dis 21:181-188.
16. Chung EK, Bian ZX, Xu HX, Sung JJ (2009) Neonatal maternal separation increases brain-derived neurotrophic factor and tyrosine kinase receptor B expression in the descending pain modulatory system. Neurosignals 17:213-221.
17. Kikusui T, Ichikawa S, Mori Y (2009) Maternal deprivation by early weaning increases corticosterone and decreases hippocampal BDNF and neurogenesis in mice. Psychoneuroendocrinology 34:762-772.
18. Macrí S, Laviola G, Leussis MP, Andersen SL (2010) Abnormal behavioral and neurotrophic development in the younger sibling receiving less maternal care in a communal nursing paradigm in rats. Psychoneuroendocrinology 35:392-402.
19. McArthur R, Borsini F (2006) Animal models of depression in drug discovery: a historical perspective. Pharmacol Biochem Behav 84:436-452. (Pubitemid 44308553)
20. Mello PB, Benetti F, Cammarota M, Izquierdo I (2009) Physical exercise can reverse the deficit in fear memory induced by maternal deprivation. Neurobiol Learn Mem 92:364-369.
21. Porsolt RD, Le Pichon M, Jalfre M (1977) Animal model of depression. Nature 266:730-732.
22. Detke MJ, Rickels M, Lucki I (1995) Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacol 121:66-72.
23. Lowry OH, Rosebough NG, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
24. El Khoury A, Gruber SH, Mork A, Mathe AA (2006) Adult life behavioral consequences of early maternal separation are alleviated by escitalopram treatment in a rat model of depression. Prog Neuropsychopharmacol Biol Psychiatry 30:535-540.
25. Aisa B, Tordera R, Lasheras B, Del Rio J, Ramirez MJ (2007) Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32: 256-266. (Pubitemid 46400278)
26. Lee JH, Kim HJ, Kim JG, Ryu V, Kim BT, Kang DW, Jahng JW (2007) Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 58:32-39. (Pubitemid 46678488)
27. Lambas-Senas L, Mnie-Filali O, Certin V, Faure C, Lemoine L, Zimmer L, Haddjeri N (2009) Functional correlates for 5-HT(1A) receptors in maternally deprived rats displaying anxiety and depression-like behaviors. Prog Neuropsychopharmacol Biol Psychiatry 33:262-268.
28. Maniam J, Morris MJ (2010) Long-term postpartum anxiety and depression-like behavior in mother rats subjected to maternal separation are ameliorated by palatable high fat diet. Behav Brain Res 208:72-79.
29. Sung Y, Shina M, Choa S, Baikb H, Jin B, Changa H, Leea E, Kima C (2010) Depression-like state in maternal rats induced by repeated separation of pups is accompanied by a decrease of cell proliferation and an increase of apoptosis in the hippocampus. Neurosci Lett 470:86-90.
30. Ruedi-Bettschen D, Pedersen EM, Feldon J, Pryce CR (2005) Early deprivation under specific conditions leads to reduced interest in reward in adulthood in Wistar rats. Behav Brain Res 156:297-310. (Pubitemid 39576070)
31. Marais L, van Rensburg SJ, van Zyl JM, Stein DJ, Daniels WM (2008) Maternal separation of rat pups increases the risk of developing depressive-like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus. Neurosci Res 61:106-112.
32. Mourlona V, Baudina A, Blanca O, Laubera A, Girosa B, Naudona L, Daugéa V (2010) Maternal deprivation induces depressive-like behaviours only in female rats. Behav Brain Res (in press).
33. Fortunato JJ, Réus GZ, Kirsch TR, Stringari RB, Fries GR, Kapczinski F, Hallak JE, Zuardi AW, Crippa JA, Quevedo J (2010) Effects of beta- carboline harmine on behavioral and physiological parameters observed in the chronic mild stress model: further evidence of antidepressant properties. Brain Res Bull 81:491-496.
34. Parker KJ, Schatzberg AF, Lyons DM (2003) Neuroendocrine aspects of hypercortisolism in major depression. Horm Behav 43: 60-66. (Pubitemid 36293275)
35. Nemeroff CB, Owens MJ (2002) Treatment of mood disorders. Nat Neurosci 5:1068-1070. (Pubitemid 35247201)
36. O'Connor TM, O'Halloran DJ, Shanahan F (2000) The stress response and the hypothalamic-pituitary-adrenal axis: from molecule to melancholia. QJM 93:323-333. (Pubitemid 30386803)
37. Rots NY, de Jong J, Workel JO, Levine S, Cools AR, de Kloet ER (1996) Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibilty to apomorphine. J Neuroendocrinol 8:501-506. (Pubitemid 26239717)
38. Mirescu C, Gould E (2006) Stress and adult neurogenesis. Hippocampus 16:233-238.
39. Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116-1127.
40. Castren E, Vooikar V, Rantamaki T (2007) Role of neurotrophic factors in depression. Curr Opin Pharmacol 7:18-21. (Pubitemid 46238033)
41. Lindsay RM, Wiegand SJ, Altar CA, DiStefano PS (1994) Neurotrophic factors: from molecule to man. Trends Neurosci 17:182-190. (Pubitemid 24128459)
42. Duman RS (2004) Role of neurotrophic factors in the etiology and treatment of mood disorders. Neuromol Med 5:11-25. (Pubitemid 38391953)
43. Kozisek ME, Middlemas D, Bylund DB (2008) Brain-derived neurotrophic factor and its receptor tropomyosin-related kinase B in the mechanism of action of antidepressant therapies. Pharmacol Ther 117:30-51. (Pubitemid 350192670)
44. Lippmann M, Bress A, Nemeroff CB, Plotsky PM, Monteggia LM (2007) Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur J Neurosci 25:3091-3098. (Pubitemid 46888796)
45. Ognibene E, Adriani W, Caprioli A, Ghirardi O, Ali SF, Aloe L, Laviola G (2008) The effect of early maternal separation on brain derived neurotrophic factor and monoamine levels in adult heterozygous realer mice. Prog Neuropsychopharmacol Biol Psychiatry 32:1269-1276.
46. Choy KH, de Visser Y, Nichols NR, van den Buuse M (2008) Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus 18:655-667. (Pubitemid 352032391)
47. Kuma H, Miki T, Matsumoto Y, Gu H, Lib H, Kusaka T, Satriotomo I, Okamoto H, Yokoyama T, Bedid KS, Onishie S, Suwakia H, Takeuchi Y (2004) Early maternal deprivation induces alterations in brain-derived neurotrophic factor expression in the developing rat hippocampus. Neurosci Lett 372:68-73. (Pubitemid 39505230)
48. Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva MA (2002) Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 7:609-616.
49. Zimmerberg B, Foote HE, Van Kempen TA (2009) Olfactory association learning and brain-derived neurotrophic factor in an animal model of early deprivation. Dev Psychobiol 51:333-344.
50. Cirulli F, Alleva E, Antonelli A, Aloe L (2000) NGF expression in the developing rat brain effects of maternal separation. Brain Res Dev Brain Res 123:129-134.
51. Schaaf MJM, Workel JO, Lesscher HM, Vreugdenhil E, Oitzl MS, de Kloet ER (2001) Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats. Brain Res 915:227-233. (Pubitemid 32947038)
52. Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237:1154-1162. (Pubitemid 17124912)
53. Cook SC, Wellman CL (2004) Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60: 236-248. (Pubitemid 39006996)
54. Maroun M, Richter-Levin G (2003) Exposure to acute stress blocks the induction of long-term potentiation of the amygdalaprefrontal cortex pathway in vivo. J Neurosci 23:4406-4409. (Pubitemid 36706170)
55. Maroun M (2006) Stress reverses plasticity in the pathway projecting from the ventromedial prefrontal cortex to the basolateral amygdala. Eur J Neurosci 24:2917-2922. (Pubitemid 44813842)
56. Petrovich GD, Holland PC, Gallagher M (2005) Amygdalar and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J Neurosci 25:8295-8302. (Pubitemid 41292124)
57. Paton JJ, Belova MA, Morrison SE, Salzman CD (2006) The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439:865-870. (Pubitemid 43255706)