Anxiety induced by prenatal stress is associated with suppression of hippocampal genes involved in synaptic function

Journal of Neurochemistry

Volumn 101, Issue 4, 2007, Pages 1018-1030

  Bogoch, Y ^a   Biala, Y N ^b   Linial, M ^a   Weinstock, M ^b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Anxiety; Exocytosis; Gene annotation; Handling; Micro array; Synapse

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENE EXPRESSION; GENE REPRESSION; HIPPOCAMPUS; NERVE FIBER GROWTH; NEUROTRANSMITTER RELEASE; NONHUMAN; PRENATAL STRESS; PRIORITY JOURNAL; PROGENY; RAT; SYNAPSE VESICLE;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SEX FACTORS; STRESS; SYNAPSES;

ANIMALIA; RATTUS;

EID: 34247556578     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04402.x     Document Type: Article

References (72)

1. Ader R. (1970) The effects of early experience on the adrenocortical response to different magnitudes of stimulation. Physiol. Behav. 5, 837 839.
2. Alonso S. J., Arevalo R., Afonso D. Rodriguez M. (1991) Effects of maternal stress during pregnancy on forced swimming test behavior of the offspring. Physiol. Behav. 50, 511 517.
3. Bayer S. A., Altman J., Russo R. J. Zhang X. (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14, 83 144.
4. Belzung C. (1992) Hippocampal mossy fibres: implication in novelty reactions or in anxiety behaviours Behav. Brain Res. 51, 149 155.
5. Berger M. A., Barros V. G., Sarchi M. I., Tarazi F. I. Antonelli M. C. (2002) Long-term effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. Neurochem. Res. 27, 1525 1533.
6. Camon E., Barrell D., Lee V., Dimmer E. Apweiler R. (2004) The Gene Ontology Annotation (GOA) Database - an integrated resource of GO annotations to the UniProt Knowledgebase. In Silico Biol. 4, 5 6.
7. Campbell S. MacQueen G. (2004) The role of the hippocampus in the pathophysiology of major depression. J. Psychiatry Neurosci. 29, 417 426.
8. Chen D., Xu W., He P., Medrano E. E. Whiteheart S. W. (2001) Gaf-1, a gamma-SNAP-binding protein associated with the mitochondria. J. Biol. Chem. 276, 13 127 13 135.
9. Coe C. L., Kramer M., Czeh B., Gould E., Reeves A. J., Kirschbaum C. Fuchs E. (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol. Psychiatry 54, 1025 1034.
10. De Bellis M. D., Casey B. J., Dahl R. E. et al. (2000) A pilot study of amygdala volumes in pediatric generalized anxiety disorder. Biol. Psychiatry 48, 51 57.
11. Dean C. Dresbach T. (2006) Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci. 29, 21 29.
12. Dennis G. Jr., Sherman B. T., Hosack D. A., Yang J., Gao W., Lane H. C. Lempicki R. A. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P 3.
13. Fride E. Weinstock M. (1988) Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci. 42, 1059 1065.
14. Fride E., Dan Y., Feldon J., Halevy G. Weinstock M. (1986) Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol. Behav. 37, 681 687.
15. Geddes J. (1999) Prenatal and perinatal risk factors for early onset schizophrenia, affective psychosis, and reactive psychosis. BMJ 318, 426.
16. Gentsch C., Lichtsteiner M., Frischknecht H. R., Feer H. Siegfried B. (1988) Isolation-induced locomotor hyperactivity and hypoalgesia in rats are prevented by handling and reversed by resocialization. Physiol. Behav. 43, 13 16.
17. Grabs D., Bergmann M. Rager G. (2000) Developmental expression of amphiphysin in the retinotectal system of the chick: from mRNA to protein. Eur. J. Neurosci. 12, 1545 1553.
18. Gué M., Bravard A., Meunier J., Veyrier R., Gaillet S., Recasens M. Maurice T. (2004) Sex differences in learning deficits induced by prenatal stress in juvenile rats. Behav. Brain Res. 150, 149 157.
19. Handley S. L. Mithani S. (1984) Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of 'fear'-motivated behaviour. Naunyn Schmiedebergs Arch. Pharmacol. 327, 1 5.
20. Hayashi A., Nagaoka M., Yamada K., Ichitani Y., Miake Y. Okado N. (1998) Maternal stress induces synaptic loss and developmental disabilities of offspring. Int. J. Dev. Neurosci. 16, 209 216.
21. Igarashi M., Tagaya M. Komiya Y. (1997) The soluble N-ethylmaleimide- sensitive factor attached protein receptor complex in growth cones: molecular aspects of the axon terminal development. J. Neurosci. 17, 1460 1470.
22. Irie F., Okuno M., Pasquale E. B. Yamaguchi Y. (2005) EphrinB-EphB signalling regulates clathrin-mediated endocytosis through tyrosine phosphorylation of synaptojanin 1. Nat. Cell Biol. 7, 501 509.
23. Jeng C. J., Chang C. C. Tang C. Y. (2005) Differential localization of rat Eag1 and Eag2 K+ channels in hippocampal neurons. Neuroreport 16, 229 233.
24. Kanai Y., Dohmae N. Hirokawa N. (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43, 513 525.
25. Keshet G. I. Weinstock M. (1995) Maternal naltrexone prevents morphological and behavioral alterations induced in rats by prenatal stress. Pharmacol. Biochem. Behav. 50, 413 419.
26. Kim E. Sheng M. (2004) PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771 781.
27. Kinnunen A. K., Koenig J. I. Bilbe G. (2003) Repeated variable prenatal stress alters pre- and postsynaptic gene expression in the rat frontal pole. J. Neurochem. 86, 736 748.
28. Kittler J. T., Thomas P., Tretter V., Bogdanov Y. D., Haucke V., Smart T. G. Moss S. J. (2004) Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating gamma-aminobutyric acid type A receptor membrane trafficking. Proc. Natl Acad. Sci. USA 101, 12 736 12 741.
29. Kuehner C. (1999) Gender differences in the short-term course of unipolar depression in a follow-up sample of depressed inpatients. J. Affect. Disord. 56, 127 139.
30. Lazzell D. R., Belizaire R., Thakur P., Sherry D. M. Janz R. (2004) SV2B regulates synaptotagmin 1 by direct interaction. J. Biol. Chem. 279, 52 124 52 131.
31. Lein E. S., Zhao X. Gage F. H. (2004) Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J. Neurosci. 24, 3879 3889.
32. 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, 11 032 11 037.
33. Levine S., Haltmeyer G. C., Karas G. G. Denenberg V. H. (1967) Physiological and behavioral effects of infantile stimulation Physiol. Behav. 2, 55 59.
34. Linial M. Parnas D. (1996) Deciphering neuronal secretion: tools of the trade. Biochim. Biophys. Acta 1286, 117 152.
35. Linnet K. M., Dalsgaard S., Obel C. et al. (2003) Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am. J. Psychiatry 160, 1028 1040.
36. Liu Z., Chatterjee T. K. Fisher R. A. (2002) RGS6 interacts with SCG10 and promotes neuronal differentiation. Role of the G gamma subunit-like (GGL) domain of RGS6. J. Biol. Chem. 277, 37 832 37 839.
37. Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A. R., Cinque C. Van Reeth O. (2003) Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci. Biobehav. Rev. 27, 119 127.
38. Marcondes F. K., Miguel K. J., Melo L. L. Spadari-Bratfisch R. C. (2001) Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol. Behav. 74, 435 440.
39. Martinez-Arca S., Proux-Gillardeaux V., Alberts P., Louvard D. Galli T. (2003) Ectopic expression of syntaxin 1 in the ER redirects TI-VAMP- and cellubrevin-containing vesicles. J. Cell Sci. 116, 2805 2816.
40. McMahon H. T., Missler M., Li C. Sudhof T. C. (1995) Complexins: cytosolic proteins that regulate SNAP receptor function. Cell 83, 111 119.
41. McMahon H. T., Bolshakov V. Y., Janz R., Hammer R. E., Siegelbaum S. A. Sudhof T. C. (1996) Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc. Natl Acad. Sci. USA 93, 4760 4764.
42. Milberger S., Biederman J., Faraone S. V., Guite J. Tsuang M. T. (1997) Pregnancy, delivery and infancy complications and attention deficit hyperactivity disorder: issues of gene-environment interaction. Biol. Psychiatry 41, 65 75.
43. Mossessova E., Bickford L. C. Goldberg J. (2003) SNARE selectivity of the COPII coat. Cell 114, 483 495.
44. O'Callaghan D. W., Haynes L. P. Burgoyne R. D. (2005) High-affinity interaction of the N-terminal myristoylation motif of the neuronal calcium sensor protein hippocalcin with phosphatidylinositol 4,5-bisphosphate. Biochem. J. 391, 231 238.
45. O'Donovan K. J., Tourtellotte W. G., Millbrandt J. Baraban J. M. (1999) The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci. 22, 167 173.
46. Oda K., Shiratsuchi T., Nishimori H., Inazawa J., Yoshikawa H., Taketani Y., Nakamura Y. Tokino T. (1999) Identification of BAIAP2 (BAI-associated protein 2), a novel human homologue of hamster IRSp53, whose SH3 domain interacts with the cytoplasmic domain of BAI1. Cytogenet. Cell Genet. 84, 75 82.
47. Okada Y., Yamazaki H., Sekine-Aizawa Y. Hirokawa N. (1995) The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81, 769 780.
48. van Os J. Selten J. P. (1998) Prenatal exposure to maternal stress and subsequent schizophrenia: the May 1940 invasion of the Netherlands. Br. J. Psychiatry 172, 324 326.
49. Paggi P. Petrucci T. C. (1992) Neuronal compartments and axonal transport of synapsin I. Mol. Neurobiol. 6, 239 251.
50. Pellow S. File S. E. (1986) Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol. Biochem. Behav. 24, 525 529.
51. Poltyrev T. Weinstock M. (2004) Gender difference in the prevention of hyperanxiety in adult prenatally stressed rats by chronic treatment with amitriptyline. Psychopharmacology (Berl.) 171, 270 276.
52. Racz B. Weinberg R. J. (2004) The subcellular organization of cortactin in hippocampus. J. Neurosci. 24, 10 310 10 317.
53. Salm A. K., Pavelko M., Krouse E. M., Webster W., Kraszpulski M. Birkle D. L. (2004) Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress. Brain Res. Dev. Brain Res. 148, 159 167.
54. Schmitz C., Rhodes M. E., Bludau M., Kaplan S., Ong P., Ueffing I., Vehoff J., Korr H. Frye C. A. (2002) Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol. Psychiatry 7, 810 813.
55. Schneider M. L. (1992) Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Dev. Psychobiol. 25, 529 540.
56. Shang W. H., Adachi Y., Nakamura A., Copeland T., Kim S. R. Kamata T. (2004) Regulation of amphiphysin1 by mitogen-activated protein kinase: its significance in nerve growth factor receptor-mediated endocytosis. J. Biol. Chem. 279, 40 890 40 896.
57. Short B., Preisinger C., Korner R., Kopajtich R., Byron O. Barr F. A. (2001) A GRASP55-rab2 effector complex linking Golgi structure to membrane traffic. J. Cell Biol. 155, 877 883.
58. Sousa R., Tannery N. H., Zhou S. Lafer E. M. (1992) Characterization of a novel synapse-specific protein. I. Developmental expression and cellular localization of the F1-20 protein and mRNA. J. Neurosci. 12, 2130 2143.
59. Stevens C. F. Sullivan J. M. (2003) The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39, 299 308.
60. Sudhof T. C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509 547.
61. Sudhof T. C., Baumert M., Perin M. S. Jahn R. (1989) A synaptic vesicle membrane protein is conserved from mammals to Drosophila. Neuron 2, 1475 1481.
62. Vallee M., Mayo W., Dellu F., Le Moal M., Simon H. Maccari S. (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 17, 2626 2636.
63. Valtorta F., Pennuto M., Bonanomi D. Benfenati F. (2004) Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis Bioessays 26, 445 453.
64. Verhage M., Maia A. S., Plomp J. J. et al. (2000) Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864 869.
65. Wakshlak A. Weinstock M. (1990) Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol. Behav. 48, 289 292.
66. Ward H. E., Johnson E. A., Salm A. K. Birkle D. L. (2000) Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiol. Behav. 70, 359 366.
67. Weaver I. C., Meaney M. J. Szyf M. (2006) Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc. Natl Acad. Sci. USA 103, 3480 3485.
68. Weinstock M. (1997) Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis Neurosci. Biobehav. Rev. 21, 1 10.
69. Weinstock M. (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog. Neurobiol. 65, 427 451.
70. Zhang B., Schmoyer D., Kirov S. Snoddy J. (2004) GOTree Machine (GOTM): a web-based platform for interpreting sets of interesting genes using Gene Ontology hierarchies. BMC Bioinformatics 5, 16.
71. Zhu Z., Li X., Chen W., Zhao Y., Li H., Qing C., Jia N., Bai Z. Liu J. (2004) Prenatal stress causes gender-dependent neuronal loss and oxidative stress in rat hippocampus. J. Neurosci. Res. 78, 837 844.
72. Ziv N. E. Garner C. C. (2004) Cellular and molecular mechanisms of presynaptic assembly. Nat. Rev. Neurosci. 5, 385 399.