Prenatal stress diminishes gender differences in behavior and in expression of hippocampal synaptic genes and proteins in rats

Hippocampus

Volumn 21, Issue 10, 2011, Pages 1114-1125

  Biala, Ya'arit Nachum ^a   Bogoch, Yoel ^b   Bejar, Corina ^a   Linial, Michal ^b   Weinstock, Marta ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

PSD95; Rab proteins; Sexual dimorphic behavior; Synaptic transmission; Synaptopodin

Indexed keywords

ARC PROTEIN; DOC2B PROTEIN; L19 PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NLGN3 PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN; RAB PROTEIN; RAB15 PROTEIN; RAB27B PROTEIN; RAB30 PROTEIN; RAB35 PROTEIN; RAB5B PROTEIN; RAB5C PROTEIN; RIMS4 PROTEIN; SYNAPTOPHYSIN; SYNAPTOPODIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATION TRANSPORT; CELL ACTIVITY; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; DOWN REGULATION; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION; GENE REPRESSION; HIPPOCAMPUS; MALE; MAZE TEST; MICROTUBULE; MITOCHONDRION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEURITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREGNANCY; PRENATAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECOGNITION; RNA TRANSLATION; SEX DIFFERENCE; SEXUAL BEHAVIOR;

ANIMALS; DOWN-REGULATION; FEMALE; GENE EXPRESSION PROFILING; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MAZE LEARNING; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RAB GTP-BINDING PROTEINS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RECOGNITION (PSYCHOLOGY); SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; SYNAPTIC TRANSMISSION; VESICULAR TRANSPORT PROTEINS;

EID: 80053112129     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20825     Document Type: Article

References (64)

1. Barbazanges A, Piazza PV, Le Moal M, Maccari S. 1996. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16: 3943-3949.
2. Bayer SA, Altman J, Russo RJ, Zhang X. 1993. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14: 83-144.
3. Bogoch Y, Biala YN, Linial M, Weinstock M. 2007. Anxiety induced by prenatal stress is associated with suppression of hippocampal genes involved in synaptic function. J Neurochem 101: 1018-1030.
4. Bosch OJ, Kromer SA, Neumann ID. 2006. Prenatal stress: Opposite effects on anxiety and hypothalamic expression of vasopressin and corticotropin-releasing hormone in rats selectively bred for high and low anxiety. Eur J Neurosci 23: 541-551.
5. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M. 1992. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70: 715-728.
6. Burns ME, Augustine GJ. 1995. Synaptic structure and function: Dynamic organization yields architectural precision. Cell 83: 187-194.
7. Cai Q, Pan PY, Sheng ZH. 2007. Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J Neurosci 27: 7284-7296.
8. 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.
9. Chen YA, Scales SJ, Scheller RH. 2001. Sequential SNARE assembly underlies priming and triggering of exocytosis. Neuron 30: 161-170.
10. Cline HT. 2001. Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11: 118-126.
11. Deacon RM, Bannerman DM, Rawlins JN. 2002. Anxiolytic effects of cytotoxic hippocampal lesions in rats. Behav Neurosci 116: 494-497.
12. Dennis G, Jr., Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. 2003. DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol 4: P3
13. Devries GJ. 1990. Sex-Differences in neurotransmitter systems. J Neuroendocrinol 2: 1-13.
14. Draghici S, Khatri P, Eklund AC, Szallasi Z. 2006. Reliability and reproducibility issues in DNA microarray measurements. Trends Genet 22: 101-109.
15. Ennaceur A, Delacour J. 1988. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31: 47-59.
16. Fernandez SM, Lewis MC, Pechenino AS, Harburger LL, Orr PT, Gresack JE, Schafe GE, Frick KM. 2008. Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J Neurosci 28: 8660-8667.
17. Fride E, Weinstock M. 1988. Prenatal stress increases anxiety-related behavior and alters cerebral lateralization of dopamine activity. Life Sci 42: 1059-1065.
18. Gomi H, Mori K, Itohara S, Izumi T. 2007. Rab27b is expressed in a wide range of exocytic cells and involved in the delivery of secretory granules near the plasma membrane. Mol Biol Cell 18: 4377-4386.
19. Handley SL, 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. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
21. Johnston AL, File SE. 1991. Sex differences in animal tests of anxiety. Physiol Behav 49: 245-250.
22. Landgraf R, Wigger A. 2002. High vs low anxiety-related behavior rats: An animal model of extremes in trait anxiety. Behav Genet 32: 301-314.
23. Li JS, Chao YS. 2008. Electrolytic lesions of dorsal CA3 impair episodic-like memory in rats. Neurobiol Learn Mem 89: 192-198.
24. Lise MF, Wong TP, Trinh A, Hines RM, Liu L, Kang R, Hines DJ, Lu J, Goldenring JR, Wang YT and others. 2006. Involvement of myosin Vb in glutamate receptor trafficking. J Biol Chem 281: 3669-3678.
25. MacLusky NJ, Naftolin F. 1981. Sexual differentiation of the central nervous system. Science 211: 1294-1302.
26. Mandyam CD, Crawford EF, Eisch AJ, Rivier CL, Richardson HN. 2008. Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus. Dev Neurobiol 68: 575-589.
27. Marcondes FK, Miguel KJ, Melo LL, Spadari-Bratfisch RC. 2001. Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 74: 435-440.
28. Martinez-Tellez RI, Hernandez-Torres E, Gamboa C, Flores G. 2009. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse 63: 794-804.
29. Masterpasqua F, Chapman RH, Lore RK. 1976. The effects of prenatal psychological stress on the sexual behavior and reactivity of male rats. Dev Psychobiol 9: 403-411.
30. Matsumoto A. 1991. Synaptogenic action of sex steroids in developing and adult neuroendocrine brain. Psychoneuroendocrinology 16: 25-40.
31. Matthews SG. 2000. Antenatal glucocorticoids and programming of the developing CNS. Pediatr Res 47: 291-300.
32. Matus A. 2000. Actin-based plasticity in dendritic spines. Science 290: 754-758.
33. McEwen BS, Lieberburg I, Chaptal C, Krey LC. 1977. Aromatization: Important for sexual differentiation of the neonatal rat brain. Horm Behav 9: 249-263.
34. McGivern RF, Poland RE, Taylor AN, Branch BJ, Raum WJ. 1986. Prenatal stress feminizes adult male saccharin preference and maze learning: Antagonism by propranolol. Monogr Neural Sci 12: 172-178.
35. Mora S, Dussaubat N, Diaz-Veliz G. 1996. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21: 609-620.
36. Mumby DG, Gaskin S, Glenn MJ, Schramek TE, Lehmann H. 2002. Hippocampal damage and exploratory preferences in rats: Memory for objects, places, and contexts. Learn Mem 9: 49-57.
37. Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J. 2006. Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 24: 1477-1487.
38. Okubo-Suzuki R, Okada D, Sekiguchi M, Inokuchi K. 2008. Synaptopodin maintains the neural activity-dependent enlargement of dendritic spines in hippocampal neurons. Mol Cell Neurosci 38: 266-276.
39. Ordyan NE, Pivina SG. 2004. Characteristics of the behavior and stress-reactivity of the hypophyseal-adrenal system in prenatally stressed rats. Neurosci Behav Physiol 34: 569-574.
40. 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.
41. Reznikov AG, Nosenko ND. 1995. Catecholamines in steroid-dependent brain development. J Steroid Biochem Mol Biol 53: 349-353.
42. Reznikov AG, Nosenko ND, Tarasenko LV. 1999. Prenatal stress and glucocorticoid effects on the developing gender-related brain. J Steroid Biochem Mol Biol 69: 109-115.
43. Rhees RW, Al-Saleh HN, Kinghorn EW, Fkeming DE, Lephart ED. 1999. Relationship between sexual behavior and sexually dimorphic structures in the anterior hypothalamus in control and prenatally stressed male rats. Brain Res Bull 50: 193-199.
44. Richardson HN, Zorrilla EP, Mandyam CD, Rivier CL. 2006. Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendocrine profiles in adulthood. Endocrinology 147: 2506-2517.
45. Sakuma Y. 2009. Gonadal steroid action and brain sex differentiation in the rat. J Neuroendocrinol 21: 410-414.
46. Segovia S, Guillamon A, del Cerro MCR, Ortega E, Perez-Laso C, Rodriguez-Zafra M, Beyer C. 1999. The development of brain sex differences: A multisignaling process. Behav Brain Res 105: 69-80.
47. Shoham S, Bejar C, Kovalev E, Schorer-Apelbaum D, Weinstock M. 2007. Ladostigil prevents gliosis, oxidative-nitrative stress and memory deficits induced by intracerebroventricular injection of streptozotocin in rats. Neuropharmacology 52: 836-843.
48. Slotten HA, Kalinichev M, Hagan JJ, Marsden CA, Fone KC. 2006. Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: Gender-dependent effects. Brain Res 1097: 123-132.
49. Son GH, Geum D, Chung S, Kim EJ, Jo JH, Kim CM, Lee KH, Kim H, Choi S, Kim HT, et al. 2006. Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J Neurosci 26: 3309-3318.
50. Stahl B, Chou JH, Li C, Sudhof TC, Jahn R. 1996. Rab3 reversibly recruits rabphilin to synaptic vesicles by a mechanism analogous to raf recruitment by ras. EMBO J 15: 1799-1809.
51. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513-525.
52. Sutcliffe JS, Marshall KM, Neill JC. 2007. Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 177: 117-125.
53. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, Cusick A, Riley ZL, Sunkin SM, Bernard A, et al. 2008. Genomic anatomy of the hippocampus. Neuron 60: 1010-1021.
54. Vlachos A, Korkotian E, Schonfeld E, Copanaki E, Deller T, Segal M. 2009. Synaptopodin regulates plasticity of dendritic spines in hippocampal neurons. J Neurosci 29: 1017-1033.
55. Walf AA, Frye CA. 2007. Estradiol decreases anxiety behavior and enhances inhibitory avoidance and gestational stress produces opposite efefcts. Stress 10: 251-260.
56. Ward IL, Stehm KE. 1991. Prenatal stress feminizes juvenile play patterns in male rats. Physiol Behav 50: 601-605.
57. Ward IL, Weisz J. 1984. Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology 114: 1635-1644.
58. Weinstock M. 2007. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 32: 1730-1740.
59. Weinstock M. 2008. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32: 1073-1086.
60. Weisz J, Brown BL, Ward IL. 1982. Maternal stress decreases steroid aromatase activity in brains of male and female rat fetuses. Neuroendocrinology 35: 374-379.
61. Yaka R, Salomon S, Matzner H, Weinstock M. 2007. Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP, synaptic proteins in juvenile male rats. Behav Brain Res 179: 126-132.
62. Zagron G, Weinstock M. 2006. Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav Brain Res 175: 323-328.
63. Zerial M, McBride H. 2001. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107-117.
64. Zuena AR, Mairesse J, Casolini P, Cinque C, Alema GS, Morley-Fletcher S, Chiodi V, Spagnoli LG, Gradini R, Catalani A, Nicoletti F, Maccari S. 2008. Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS One 3: e2170.