Prenatal stress alters glutamatergic system responsiveness in adult rat prefrontal cortex

Journal of Neurochemistry

Volumn 109, Issue 6, 2009, Pages 1733-1744

  Fumagalli, Fabio ^b   Pasini, Matteo ^b,c   Frasca, Angelisa ^b   Drago, Filippo ^c   Racagni, Giorgio ^b,d   Riva, Marco Andrea ^a,b  

^a Center of Neuropharmacology   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF CATANIA   (Italy)

^d IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

Author keywords

calcium calmodulin dependent protein kinase II; Cognition; Hippocampus; NMDA receptors; Pregnancy; Vulnerability

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CALCIUM TRANSPORT; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; MALE; NONHUMAN; PREFRONTAL CORTEX; PRENATAL STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANALYSIS OF VARIANCE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; MALE; PHOSPHORYLATION; PREFRONTAL CORTEX; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUTAMATE; RESTRAINT, PHYSICAL; SERINE; SEX FACTORS; STRESS, PSYCHOLOGICAL; SWIMMING; THREONINE;

ANIMALIA; RATTUS;

EID: 65949113839     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06088.x     Document Type: Article

References (36)

1. Buckley P. F., Mahadik S., Pillai A. Terry A. Jr. (2007) Neurotrophins and schizophrenia. Schizophr. Res. 94, 1 11. (Pubitemid 47033973)
2. Chapman R. H. Stern J. M. (1979) Failure of severe maternal stress or ACTH during pregnancy to affect emotionality of male rat offspring: implications of litter effects for prenatal studies. Dev. Psychobiol. 12, 255 267. (Pubitemid 9141241)
3. Colbran R. J. Brown A. M. (2004) Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr. Opin. Neurobiol. 14, 318 327. (Pubitemid 38759862)
4. Deminiere J. M., Piazza P. V., Guegan G., Abrous N., Maccari S., Le Moal M. Simon H. (1992) Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res. 586, 135 139.
5. EEC Council Directive (1987) 86/609, OJL 358, 1.
6. Fong T. M., Davidson N. Lester H. A. (1989) Further evidence demonstrating that N-methyl-D-aspartate and kainate activate distinct ion channels. Synapse 4, 88 95. (Pubitemid 19195215)
7. Fride E. Weinstock M. (1988) Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci. 42, 1059 1065. (Pubitemid 18056843)
8. Fumagalli F., Bedogni F., Perez J., Racagni G. Riva M. A. (2004) Corticostriatal brain-derived neurotrophic factor dysregulation in adult rats following prenatal stress. Eur. J. Neurosci. 20, 1348 1354. (Pubitemid 39233585)
9. Fumagalli F., Bedogni F., Slotkin T. A., Racagni G. Riva M. A. (2005) Prenatal stress elicits regionally selective changes in basal FGF-2 gene expression in adulthood and alters the adult response to acute or chronic stress. Neurobiol. Dis. 20, 731 737. (Pubitemid 41619349)
10. Fumagalli F., Di Pasquale L., Caffino L., Racagni G. Riva M. A. (2007a) Repeated exposure to cocaine differently modulates BDNF mRNA and protein levels in rat striatum and prefrontal cortex. Eur. J. Neurosci. 26, 2756 2763. (Pubitemid 350115522)
11. Fumagalli F., Molteni R., Racagni G. Riva M. A. (2007b) Stress during development: impact on neuroplasticity and relevance to psychopathology. Prog. Neurobiol. 81, 197 217. (Pubitemid 46498900)
12. Henry C., Guegant G., Cador M., Arnauld E., Arsaut J., Le Moal M. Demotes-Mainard J. (1995) Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens. Brain Res. 685, 179 186.
13. Jing H., Iwasaki Y., Nishiyama M., Taguchi T., Tsugita M., Taniguchi Y., Kambayashi M. Hashimoto K. (2008) Multisignal regulation of the rat NMDA1 receptor subunit gene-a pivotal role of glucocorticoid-dependent transcription. Life Sci. 82, 1137 1141.
14. Kippin T. E., Szumlinski K. K., Kapasova Z., Rezner B. See R. E. (2008) Prenatal stress enhances responsiveness to cocaine. Neuropsychopharmacology 33, 769 782.
15. Koehl M., Lemaire V., Vallee M., Abrous N., Piazza P. V., Mayo W., Maccari S. Le Moal M. (2001) Long term neurodevelopmental and behavioral effects of perinatal life events in rats. Neurotox. Res. 3, 65 83. (Pubitemid 32717296)
16. Koenig J. I., Elmer G. I., Shepard P. D., Lee P. R., Mayo C., Joy B., Hercher E. Brady D. L. (2005) Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behav. Brain Res. 156, 251 261. (Pubitemid 39576065)
17. Lemaire V., Koehl M., Le Moal M. Abrous D. N. (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl Acad. Sci. USA 97, 11032 11037.
18. Lemaire V., Lamarque S., Le Moal M., Piazza P. V. Abrous D. N. (2006) Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol. Psychiatry 59, 786 792.
19. Louvart H., Maccari S., Vaiva G. Darnaudery M. (2009) Prenatal stress exacerbates the impact of an aversive procedure on the corticosterone response to stress in female rats. Psychoneuroendocrinology 34, 786 790.
20. Maccari S. Morley-Fletcher S. (2007) Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32 Suppl 1, S10 S15. (Pubitemid 47211641)
21. Maccari S., Piazza P. V., Kabbaj M., Barbazanges A., Simon H. Le Moal M. (1995) Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J. Neurosci. 15, 110 116.
22. Morinobu S., Fujimaki K., Kawano K., Tanaka K., Takahashi J., Ohkawa M., Yamawaki S. Kato N. (2003) Influence of immobilization stress on the expression and phosphatase activity of protein phosphatase 2A in the rat brain. Biol. Psychiatry 54, 1060 1066. (Pubitemid 37415041)
23. Olney J. W. Farber N. B. (1995) Glutamate receptor dysfunction and schizophrenia. Arch. Gen. Psychiatry 52, 998 1007.
24. Paxinos G. Watson C. (1996) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York, NY.
25. Riva M. A., Molteni R., Bedogni F., Racagni G. Fumagalli F. (2005) Emerging role of the FGF system in psychiatric disorders. Trends Pharmacol. Sci. 26, 228 231. (Pubitemid 40603070)
26. Russo S. J., Mazei-Robison M. S., Ables J. L. Nestler E. J. (2009) Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 56(S1), 73 82.
27. Son G. H., Geum D., Chung S. et al. (2006) Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J. Neurosci. 26, 3309 3318.
28. Spauwen J., Krabbendam L., Lieb R., Wittchen H. U. van Os J. (2004) Early maternal stress and health behaviours and offspring expression of psychosis in adolescence. Acta Psychiatr. Scand. 110, 356 364. (Pubitemid 39424837)
29. Strack S., McNeill R. B. Colbran R. J. (2000) Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 275, 23798 23806. (Pubitemid 30624665)
30. Suenaga T., Morinobu S., Kawano K., Sawada T. Yamawaki S. (2004) Influence of immobilization stress on the levels of CaMKII and phospho-CaMKII in the rat hippocampus. Int. J. Neuropsychopharmacol. 7, 299 309. (Pubitemid 39166464)
31. Szabo S. T., Machado-Vieira R., Yuan P. et al. (2009) Glutamate receptors as targets of protein kinase C in the pathophysiology and treatment of animal models of Mania. Neuropharmacology 56, 47 55.
32. Takahashi J., Tanaka K., Morinobu S., Fujimaki K., Li S. T., Kato K., Ohkawa M., Yamawaki S. Kato N. (2001) Influence of restraint stress on the expression and the serine/threonine phosphatase activity of calcineurin in the rat brain. Synapse 40, 130 136. (Pubitemid 32239594)
33. Weinstock M. (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog. Neurobiol. 65, 427 451. (Pubitemid 33016408)
34. Weinstock M. (2007) Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem. Res. 32, 1730 1740. (Pubitemid 47428852)
35. Weinstock M., Fride E. Hertzberg R. (1988) Prenatal stress effects on functional development of the offspring. Prog. Brain Res. 73, 319 331. (Pubitemid 18198829)
36. Zuena A. R., Mairesse J., Casolini P. et al. (2008) Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE 3, e2170.