Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression

•Effects of chronic unpredictable prenatal stress were tested in adult offspring.•Prenatal stress impaired spatial memory in adult male and female offspring.•Prenatally stressed females had less H3 acetylation and higher DNMT1 levels.•Prenatally stressed females had higher plasma corticosterone leve...

Celý popis

Uloženo v:

Podrobná bibliografie
Vydáno v:	Behavioural brain research Ročník 281; s. 1 - 8
Hlavní autoři:	Benoit, Jamie D., Rakic, Pasko, Frick, Karyn M.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	Netherlands Elsevier B.V 15.03.2015
Témata:	Acetylation Animals Chronic unpredictable stress Corticosterone - blood DNA (Cytosine-5-)-Methyltransferase 1 DNA (Cytosine-5-)-Methyltransferases - genetics DNA methyltransferase Epigenesis, Genetic Female Gene Expression Heterochromatin - metabolism Hippocampus - metabolism Histone acetylation Histones - genetics Male Maze Learning Memory Disorders Mice Mice, Inbred C57BL Morris water maze Mouse Pregnancy Prenatal Exposure Delayed Effects - genetics Prenatal Exposure Delayed Effects - psychology Risk Factors Sex differences Sex Factors Spatial Memory Stress, Psychological - blood Stress, Psychological - complications Stress, Psychological - genetics Stress, Psychological - psychology Chronic unpredictable stress Sex differences DNA methyltransferase Histone acetylation Morris water maze Mouse
ISSN:	0166-4328, 1872-7549, 1872-7549
On-line přístup:	Získat plný text
Tagy:	Přidat tag Žádné tagy, Buďte první, kdo vytvoří štítek k tomuto záznamu!

Abstract	•Effects of chronic unpredictable prenatal stress were tested in adult offspring.•Prenatal stress impaired spatial memory in adult male and female offspring.•Prenatally stressed females had less H3 acetylation and higher DNMT1 levels.•Prenatally stressed females had higher plasma corticosterone levels than males.•The female brain may be more susceptible to the effects of prenatal stress. Stress during pregnancy has a wide variety of negative effects in both human [1] and animal offspring [2]. These effects are especially apparent in various forms of learning and memory such as object recognition [3] and spatial memory [4]. The cognitive effects of prenatal stress (PNS) may be mediated through epigenetic changes such as histone acetylation and DNA methylation [5]. As such, the present study investigated the effects of chronic unpredictable PNS on memory and epigenetic measures in adult offspring. Mice that underwent PNS exhibited impaired spatial memory in the Morris water maze, as well as sex-specific changes in levels of DNA methyltransferase (DNMT) 1 protein, and acetylated histone H3 (AcH3) in the hippocampus, and serum corticosterone. Male mice exposed to PNS exhibited decreased hippocampal AcH3, whereas female PNS mice displayed a further reduction in AcH3, as well as heightened hippocampal DNMT1 protein levels and corticosterone levels. These data suggest that PNS may epigenetically reduce transcription in the hippocampus, particularly in females in whom this effect may be related to increased baseline stress hormone levels, and which may underlie the sexual dimorphism in rates of mental illness in humans.
AbstractList	•Effects of chronic unpredictable prenatal stress were tested in adult offspring.•Prenatal stress impaired spatial memory in adult male and female offspring.•Prenatally stressed females had less H3 acetylation and higher DNMT1 levels.•Prenatally stressed females had higher plasma corticosterone levels than males.•The female brain may be more susceptible to the effects of prenatal stress. Stress during pregnancy has a wide variety of negative effects in both human [1] and animal offspring [2]. These effects are especially apparent in various forms of learning and memory such as object recognition [3] and spatial memory [4]. The cognitive effects of prenatal stress (PNS) may be mediated through epigenetic changes such as histone acetylation and DNA methylation [5]. As such, the present study investigated the effects of chronic unpredictable PNS on memory and epigenetic measures in adult offspring. Mice that underwent PNS exhibited impaired spatial memory in the Morris water maze, as well as sex-specific changes in levels of DNA methyltransferase (DNMT) 1 protein, and acetylated histone H3 (AcH3) in the hippocampus, and serum corticosterone. Male mice exposed to PNS exhibited decreased hippocampal AcH3, whereas female PNS mice displayed a further reduction in AcH3, as well as heightened hippocampal DNMT1 protein levels and corticosterone levels. These data suggest that PNS may epigenetically reduce transcription in the hippocampus, particularly in females in whom this effect may be related to increased baseline stress hormone levels, and which may underlie the sexual dimorphism in rates of mental illness in humans. Stress during pregnancy has a wide variety of negative effects in both human [1] and animal offspring [2]. These effects are especially apparent in various forms of learning and memory such as object recognition [3] and spatial memory [4]. The cognitive effects of prenatal stress (PNS) may be mediated through epigenetic changes such as histone acetylation and DNA methylation [5]. As such, the present study investigated the effects of chronic unpredictable PNS on memory and epigenetic measures in adult offspring. Mice that underwent PNS exhibited impaired spatial memory in the Morris water maze, as well as sex-specific changes in levels of DNA methyltransferase (DNMT) 1 protein, and acetylated histone H3 (AcH3) in the hippocampus, and serum corticosterone. Male mice exposed to PNS exhibited decreased hippocampal AcH3, whereas female PNS mice displayed a further reduction in AcH3, as well as heightened hippocampal DNMT1 protein levels and corticosterone levels. These data suggest that PNS may epigenetically reduce transcription in the hippocampus, particularly in females in whom this effect may be related to increased baseline stress hormone levels, and which may underlie the sexual dimorphism in rates of mental illness in humans. Stress during pregnancy has a wide variety of negative effects in both human [1] and animal offspring [2]. These effects are especially apparent in various forms of learning and memory such as object recognition [3] and spatial memory [4]. The cognitive effects of prenatal stress (PNS) may be mediated through epigenetic changes such as histone acetylation and DNA methylation [5]. As such, the present study investigated the effects of chronic unpredictable PNS on memory and epigenetic measures in adult offspring. Mice that underwent PNS exhibited impaired spatial memory in the Morris water maze, as well as sex-specific changes in levels of DNA methyltransferase (DNMT) 1 protein, and acetylated histone H3 (AcH3) in the hippocampus, and serum corticosterone. Male mice exposed to PNS exhibited decreased hippocampal AcH3, whereas female PNS mice displayed a further reduction in AcH3, as well as heightened hippocampal DNMT1 protein levels and corticosterone levels. These data suggest that PNS may epigenetically reduce transcription in the hippocampus, particularly in females in whom this effect may be related to increased baseline stress hormone levels, and which may underlie the sexual dimorphism in rates of mental illness in humans.Stress during pregnancy has a wide variety of negative effects in both human [1] and animal offspring [2]. These effects are especially apparent in various forms of learning and memory such as object recognition [3] and spatial memory [4]. The cognitive effects of prenatal stress (PNS) may be mediated through epigenetic changes such as histone acetylation and DNA methylation [5]. As such, the present study investigated the effects of chronic unpredictable PNS on memory and epigenetic measures in adult offspring. Mice that underwent PNS exhibited impaired spatial memory in the Morris water maze, as well as sex-specific changes in levels of DNA methyltransferase (DNMT) 1 protein, and acetylated histone H3 (AcH3) in the hippocampus, and serum corticosterone. Male mice exposed to PNS exhibited decreased hippocampal AcH3, whereas female PNS mice displayed a further reduction in AcH3, as well as heightened hippocampal DNMT1 protein levels and corticosterone levels. These data suggest that PNS may epigenetically reduce transcription in the hippocampus, particularly in females in whom this effect may be related to increased baseline stress hormone levels, and which may underlie the sexual dimorphism in rates of mental illness in humans.
Author	Rakic, Pasko Frick, Karyn M. Benoit, Jamie D.
AuthorAffiliation	c Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, WI 53211, United States b Department of Neurobiology, Yale University School of Medicine, New Haven, CT 06520, United States a Department of Psychology, Yale University, New Haven, CT 06520, United States
AuthorAffiliation_xml	– name: c Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, WI 53211, United States – name: a Department of Psychology, Yale University, New Haven, CT 06520, United States – name: b Department of Neurobiology, Yale University School of Medicine, New Haven, CT 06520, United States
Author_xml	– sequence: 1 givenname: Jamie D. surname: Benoit fullname: Benoit, Jamie D. organization: Department of Psychology, Yale University, New Haven, CT 06520, United States – sequence: 2 givenname: Pasko surname: Rakic fullname: Rakic, Pasko organization: Department of Neurobiology, Yale University School of Medicine, New Haven, CT 06520, United States – sequence: 3 givenname: Karyn M. surname: Frick fullname: Frick, Karyn M. email: frickk@uwm.edu organization: Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, WI 53211, United States
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25496779$$D View this record in MEDLINE/PubMed
BookMark	eNqNUsFu1DAUtFAR3RY-gAvykUuCHcdxIiQkVNGCVAkOcLYc-2XjVWIH27uiH8O_4uy2CDhUnGz5zYxHb-YCnTnvAKGXlJSU0ObNruz7UFaE1iWtSkLoE7ShragKwevuDG0ypilqVrXn6CLGHSGkJpw-Q-dVnjdCdBv080sAp5KacEwBYsTWmb2GiOOiks3PM8w-3GEDg9U2RaycwbDYLThIVmM9KreFlYbTCHi0y-K1mpf9UcnqLHIA7Ac8QoLg9Rj8nN8cHnxYL94dFQOsvxq8ymL4saxW8uw5ejqoKcKL-_MSfbv-8PXqY3H7-ebT1fvbQnNOUmFaTQcmmgoocEOYaClnXWeqgbTG6Ib1ILThtRBKicoYRnuiVduTGtjQ1pxdoncn3WXfz2A0uBTUJJdgZxXupFdW_j1xdpRbf5A1I3mVJAu8vhcI_vseYpKzjRqmSTnw-yhpIxhrKSPsP6C8qhnt-Grr1Z-2fvt5iC8DxAmgg48xwCBzRsetZpd2kpTItShyJ3NR5FoUSSuZi5KZ9B_mg_hjnLcnDuQoDhaCjNqCy7nZADpJ4-0j7F-Kedrp
CitedBy_id	crossref_primary_10_1038_s41598_017_03373_w crossref_primary_10_4103_1673_5374_239443 crossref_primary_10_1016_j_envpol_2025_125860 crossref_primary_10_1371_journal_pone_0302374 crossref_primary_10_1016_j_neubiorev_2018_05_026 crossref_primary_10_1016_j_brainresbull_2019_08_020 crossref_primary_10_1017_S095457941600081X crossref_primary_10_1038_s41398_021_01639_6 crossref_primary_10_1016_j_jpsychires_2022_03_032 crossref_primary_10_1038_s41598_017_01811_3 crossref_primary_10_1111_sji_12919 crossref_primary_10_1007_s12038_021_00153_7 crossref_primary_10_1016_j_cobeha_2018_05_007 crossref_primary_10_1016_j_neurobiolaging_2021_12_006 crossref_primary_10_1016_j_nlm_2016_08_009 crossref_primary_10_1016_j_psyneuen_2022_105661 crossref_primary_10_1016_j_ijdevneu_2018_11_007 crossref_primary_10_1016_j_bbii_2025_100108 crossref_primary_10_1038_mp_2017_35 crossref_primary_10_1016_j_neubiorev_2023_105194 crossref_primary_10_1016_j_neulet_2024_137886 crossref_primary_10_1097_FBP_0000000000000682 crossref_primary_10_3390_ph9010009 crossref_primary_10_1016_j_ynstr_2025_100736 crossref_primary_10_1016_j_neuro_2017_07_002 crossref_primary_10_3390_ijms21165627 crossref_primary_10_1016_j_yhbeh_2018_01_004 crossref_primary_10_1016_j_physbeh_2021_113314 crossref_primary_10_1016_j_expneurol_2016_07_002 crossref_primary_10_1080_15592294_2016_1145329 crossref_primary_10_1016_j_bbr_2015_11_031 crossref_primary_10_1016_j_earlhumdev_2020_105190 crossref_primary_10_1002_jdn_10052 crossref_primary_10_1038_s41380_025_03258_9 crossref_primary_10_1002_dev_21834 crossref_primary_10_1371_journal_pone_0191563 crossref_primary_10_1097_WNR_0000000000000552 crossref_primary_10_3389_fnhum_2021_635304 crossref_primary_10_1002_jnr_23864 crossref_primary_10_1371_journal_pone_0180306 crossref_primary_10_1038_s41380_019_0366_8 crossref_primary_10_1016_j_neubiorev_2022_104627 crossref_primary_10_1134_S1819712419020065 crossref_primary_10_1002_jdn_10001 crossref_primary_10_1016_j_expneurol_2017_09_001 crossref_primary_10_1016_j_ntt_2017_12_009 crossref_primary_10_1016_j_ntt_2020_106914 crossref_primary_10_1007_s11064_017_2206_z crossref_primary_10_1027_2151_2604_a000219 crossref_primary_10_3390_ijms25042211 crossref_primary_10_1007_s12035_023_03348_1 crossref_primary_10_1093_eep_dvw007 crossref_primary_10_1177_1545968319834898 crossref_primary_10_1017_neu_2020_3 crossref_primary_10_1016_j_anbehav_2022_09_015 crossref_primary_10_1186_s13041_016_0197_3 crossref_primary_10_1007_s11055_023_01355_2 crossref_primary_10_3390_ijms26073028 crossref_primary_10_1134_S1819712417040109 crossref_primary_10_3389_fcell_2021_657591 crossref_primary_10_1016_j_neubiorev_2017_05_016 crossref_primary_10_1016_j_tig_2022_03_006 crossref_primary_10_1016_j_neuroscience_2018_03_043 crossref_primary_10_1007_s11055_022_01231_5 crossref_primary_10_1093_icb_icv029 crossref_primary_10_1038_s41598_017_09799_6
Cites_doi	10.1007/s00018-006-6026-6 10.1101/lm.278206 10.1101/lm.2097411 10.1016/S0166-4328(03)00250-X 10.1038/25779 10.1016/j.neurobiolaging.2012.05.012 10.1038/297681a0 10.1002/dev.420170607 10.1016/j.yhbeh.2010.05.004 10.1242/jcs.00804 10.1111/nmo.12326 10.1016/j.ijdevneu.2007.03.009 10.1074/jbc.M511767200 10.1016/j.neuropharm.2012.04.013 10.1007/BF00238949 10.1016/j.nlm.2007.07.016 10.1371/journal.pone.0039791 10.1093/nar/27.11.2291 10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7 10.1073/pnas.1107759108 10.1523/JNEUROSCI.4119-05.2005 10.1073/pnas.97.20.11032 10.1159/000335524 10.1038/nature07925 10.1016/j.brainres.2007.01.024 10.1016/j.neuroscience.2013.03.025 10.1186/1471-244X-8-71 10.1016/j.yfrne.2014.05.001 10.1016/j.neuroscience.2011.02.026 10.1038/30764 10.1016/S0031-9384(97)00456-3 10.1523/JNEUROSCI.3850-05.2006 10.1111/j.1365-2826.2010.02097.x 10.1210/en.2003-1759 10.1590/S0100-879X1999001000009 10.1002/hipo.20825 10.1016/j.siny.2008.11.002 10.1016/S0031-9384(00)00351-6 10.1016/j.brainresrev.2007.11.004 10.1016/S0149-7634(02)00015-5 10.1073/pnas.0903964106 10.1016/j.biopsych.2008.09.002 10.1038/29542 10.1016/S0166-4328(99)00122-9 10.1038/366362a0 10.1007/s10519-006-9106-3 10.1016/S0168-1591(98)00188-9 10.1073/pnas.0910578107 10.1523/JNEUROSCI.1887-11.2011 10.1016/0024-3205(85)90306-6 10.1101/lm.1986911 10.1016/0092-8674(92)90611-F 10.1523/JNEUROSCI.17-07-02626.1997 10.1037/0735-7044.107.4.627 10.1074/jbc.M402229200 10.1038/npp.2011.274 10.1002/hipo.20181 10.1046/j.1460-9568.1999.00705.x 10.1016/S0306-4522(01)00065-3 10.1038/nn.2666 10.1016/S1043-2760(02)00690-2
ContentType	Journal Article
Copyright	2014 Elsevier B.V. Copyright © 2014 Elsevier B.V. All rights reserved. 2014 Published by Elsevier B.V. 2014
Copyright_xml	– notice: 2014 Elsevier B.V. – notice: Copyright © 2014 Elsevier B.V. All rights reserved. – notice: 2014 Published by Elsevier B.V. 2014
DBID	AAYXX CITATION CGR CUY CVF ECM EIF NPM 7X8 7QG 7TK 8FD FR3 P64 RC3 5PM
DOI	10.1016/j.bbr.2014.12.001
DatabaseName	CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed MEDLINE - Academic Animal Behavior Abstracts Neurosciences Abstracts Technology Research Database Engineering Research Database Biotechnology and BioEngineering Abstracts Genetics Abstracts PubMed Central (Full Participant titles)
DatabaseTitle	CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic Genetics Abstracts Engineering Research Database Technology Research Database Neurosciences Abstracts Animal Behavior Abstracts Biotechnology and BioEngineering Abstracts
DatabaseTitleList	MEDLINE MEDLINE - Academic Genetics Abstracts
Database_xml	– sequence: 1 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database
DeliveryMethod	fulltext_linktorsrc
Discipline	Anatomy & Physiology
EISSN	1872-7549
EndPage	8
ExternalDocumentID	PMC4305490 25496779 10_1016_j_bbr_2014_12_001 S0166432814007864
Genre	Research Support, Non-U.S. Gov't Journal Article Research Support, N.I.H., Extramural
GrantInformation_xml	– fundername: NCATS NIH HHS grantid: UL1 TR000142 – fundername: NINDS NIH HHS grantid: R01 NS038296 – fundername: NINDS NIH HHS grantid: R01-NS038296 – fundername: NIDA NIH HHS grantid: R01-DA023999 – fundername: NIDA NIH HHS grantid: R37 DA023999 – fundername: NIA NIH HHS grantid: R01 AG022525 – fundername: NIDA NIH HHS grantid: R01 DA023999 – fundername: NIA NIH HHS grantid: R01-AG022525
GroupedDBID	--- --K --M .~1 0R~ 1B1 1RT 1~. 1~5 23N 4.4 457 4G. 53G 5GY 5VS 6J9 7-5 71M 8P~ 9JM AABNK AACTN AADPK AAEDT AAEDW AAIAV AAIKJ AAKOC AALRI AAOAW AAQFI AAXLA AAXUO ABCQJ ABFNM ABFRF ABIVO ABJNI ABMAC ABYKQ ACDAQ ACGFO ACGFS ACIUM ACRLP ADBBV ADEZE AEBSH AEFWE AEKER AENEX AFKWA AFTJW AFXIZ AGHFR AGUBO AGWIK AGYEJ AIEXJ AIKHN AITUG AJBFU AJOXV ALMA_UNASSIGNED_HOLDINGS AMFUW AMRAJ AXJTR BKOJK BLXMC C45 CS3 DU5 EBS EFJIC EFLBG EJD EO8 EO9 EP2 EP3 F5P FDB FIRID FNPLU FYGXN G-Q GBLVA IHE J1W KOM L7B M2V M41 MO0 MOBAO N9A O-L O9- OAUVE OVD OZT P-8 P-9 P2P PC. Q38 RIG ROL RPZ SCC SDF SDG SDP SES SPCBC SSN SSZ T5K TEORI TN5 WH7 YR2 ~G- .GJ 41~ 9DU AAQXK AATTM AAXKI AAYWO AAYXX ABWVN ABXDB ACLOT ACRPL ACVFH ADCNI ADIYS ADMUD ADNMO AEIPS AEUPX AFJKZ AFPUW AGQPQ AHHHB AI. AIGII AIIUN AKBMS AKRWK AKYEP ANKPU APXCP ASPBG AVWKF AZFZN CITATION EFKBS FEDTE FGOYB G-2 HMQ HVGLF HZ~ R2- SEW SNS VH1 WUQ ZGI ZXP ZY4 ~HD CGR CUY CVF ECM EIF NPM 7X8 7QG 7TK 8FD FR3 P64 RC3 5PM
ID	FETCH-LOGICAL-c550t-d8c1f3762e1e5d037815399d2f08ddc63be7cd5477aa72dd31b0ca8b04e3f8453
ISICitedReferencesCount	83
ISICitedReferencesURI	http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000349504600001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN	0166-4328 1872-7549
IngestDate	Tue Sep 30 16:56:13 EDT 2025 Wed Oct 01 15:00:59 EDT 2025 Sun Sep 28 09:15:28 EDT 2025 Wed Feb 19 02:30:41 EST 2025 Sat Nov 29 06:34:09 EST 2025 Tue Nov 18 21:01:51 EST 2025 Fri Feb 23 02:33:18 EST 2024
IsDoiOpenAccess	false
IsOpenAccess	true
IsPeerReviewed	true
IsScholarly	true
Keywords	Chronic unpredictable stress Sex differences DNA methyltransferase Histone acetylation Morris water maze Mouse
Language	English
License	Copyright © 2014 Elsevier B.V. All rights reserved.
LinkModel	OpenURL
MergedId	FETCHMERGED-LOGICAL-c550t-d8c1f3762e1e5d037815399d2f08ddc63be7cd5477aa72dd31b0ca8b04e3f8453
Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
OpenAccessLink	https://www.ncbi.nlm.nih.gov/pmc/articles/4305490
PMID	25496779
PQID	1652431955
PQPubID	23479
PageCount	8
ParticipantIDs	pubmedcentral_primary_oai_pubmedcentral_nih_gov_4305490 proquest_miscellaneous_1673381303 proquest_miscellaneous_1652431955 pubmed_primary_25496779 crossref_citationtrail_10_1016_j_bbr_2014_12_001 crossref_primary_10_1016_j_bbr_2014_12_001 elsevier_sciencedirect_doi_10_1016_j_bbr_2014_12_001
PublicationCentury	2000
PublicationDate	2015-03-15
PublicationDateYYYYMMDD	2015-03-15
PublicationDate_xml	– month: 03 year: 2015 text: 2015-03-15 day: 15
PublicationDecade	2010
PublicationPlace	Netherlands
PublicationPlace_xml	– name: Netherlands
PublicationTitle	Behavioural brain research
PublicationTitleAlternate	Behav Brain Res
PublicationYear	2015
Publisher	Elsevier B.V
Publisher_xml	– name: Elsevier B.V
References	Mychasiuk, Gibb, Kolb (bib0280) 2011; 33 Moser, Moser (bib0235) 1998; 8 Bowman, MacLusky, Sarmiento, Frankfurt, Gordon, Luine (bib0030) 2004; 45 Biala, Bogoch, Bejar, Linial, Weinstock (bib0285) 2011; 21 Salomon, Bejar, Schorer-Apelbaum, Weinstock (bib0065) 2011; 23 Nan, Ng, Johnson, Lahgerty, Turner, Eisenman (bib0180) 1998; 393 Lemaire, Koehl, Le Moal, Abrous (bib0105) 2000; 97 Robertson, Uzvolgi, Liang, Talmadge, Sumegi, Gonzales (bib0210) 1999; 27 Malaspina, Corcoran, Kleinhaus, Perrin, Fennig, Nahon (bib0315) 2008; 8 Miller, Campbell, Sweatt (bib0125) 2008; 89 De Quervain, Roozendaal, McGaugh (bib0090) 1998; 394 Schenk, Morris (bib0225) 1985; 58 Morgan, Bale (bib0310) 2011; 31 Wood, Hawk, Abel (bib0130) 2006; 13 Cabrera, Rodriguez-Echandia, Jatuff, Foscolo (bib0015) 1999; 32 Sweatt (bib0135) 2009; 65 Sierksma, Prickaerts, Chouliaras, Rostamian, Delbroek, Rutten (bib0250) 2013; 34 Kay, Tarcic, Poltyrev, Weinstock (bib0035) 1998; 63 Haettig, Stefanko, Multani, Figueroa, McQuown, Wood (bib0155) 2011; 18 Guan, Haggarty, Giacometti, Dannenberg, Joseph, Gao (bib0150) 2009; 459 Winston, Li, Sarna (bib0255) 2014; 5 Darnaudery, Maccari (bib0080) 2008; 57 Hawk, Florian, Abel (bib0160) 2011; 18 Levenson, Sweatt (bib0115) 2005; 1 Li, Beard, Jaenisch (bib0190) 1993; 366 Levenson, Roth, Lubin, Miller, Huang, Desai (bib0205) 2006; 281 Mychasiuk, Ilnytskyy, Kovalchuk, Kolb, Gibb (bib0290) 2011; 180 Fuks, Burgers, Brehm, Hughes-Davies, Kouzarides (bib0215) 2000; 24 Son, Geum, Chung, Kim, Jo, Kim (bib0095) 2006; 26 Matrisciano, Tueting, Dalal, Kadriu, Grayson, Davis (bib0270) 2012; 68 Wellberg, Seckl, Holmes (bib0305) 2001; 104 Vallee, Maccari, Dellu, Simon, Le Moal, Mayo (bib0020) 1999; 11 Vallee, Mayo, Dellu, Le Moal, Simon, Maccari (bib0050) 1997; 17 Zhao, Fan, Frick (bib0170) 2010; 107 Entringer, Epel, Kumsta, Lin, Helhammer, Blackburn (bib0045) 2011; 108 Markham, Taylor, Taylor, Bell, Koenig (bib0060) 2010; 25 Li, Bestor, Jaenisch (bib0185) 1992; 69 Chen, Pettersson, Beard, Jackson-Grusby, Jaenisch (bib0195) 1998; 395 Fortress, Frick (bib0145) 2014; 35 Mychasiuk, Harker, Ilyntskyy, Gibb (bib0295) 2013; 241 Yang, Han, Cao, Lingjiang, Xu (bib0240) 2006; 16 Gue, Bravard, Meunier, Veyrier, Gaillet, Recasens (bib0075) 2004; 150 Jacobson, Cryan (bib0275) 2007; 1 Matthews (bib0300) 2002; 13 Wu, Song, Li, He, Ge, Wang (bib0245) 2007; 1141 Szuran, Pliska, Pokorny, Welzl (bib0070) 2000; 71 Morris, Garrud, Rawlins, O’Keefe (bib0220) 1982; 297 Kofman (bib0005) 2002; 26 Levenson, O’Riordan, Brown, Trinh, Molfese, Sweatt (bib0110) 2004; 279 Stefanko, Barrett, Ly, Reolon, Wood (bib0165) 2009; 106 Markowska, Long, Johnson, Olton (bib0230) 1993; 107 Fride, Weinstock (bib0040) 1984; 17 Braastad (bib0010) 1998; 61 Levenson, Sweatt (bib0120) 2006; 63 Mesquita, Wegerich, Patchev, Oliveira, Leao, Sousa (bib0025) 2009; 14 Colvis, Pollock, Goodman, Imprey, Dunn, Mandel (bib0140) 2005; 24 Lehmann, Stohr, Feldon (bib0055) 2000; 107 Day, Sweatt, Dunn, Morgan, Bale (bib0200) 2010; 13 Matrisciano, Tueting, Maccari, Nicoletti, Guidotti (bib0265) 2012; 4 Cai, Zhu, Huang, Li, Fan, Jia (bib0100) 2007; 25 Jensen Peña, Monk, Champagne (bib0260) 2012; 6 Crosio, Heitz, Allis, Borelli, Sassone-Corsi (bib0175) 2003; 116 Fride, Dan, Gavish, Weinstock (bib0085) 1985; 22 Haettig (10.1016/j.bbr.2014.12.001_bib0155) 2011; 18 Crosio (10.1016/j.bbr.2014.12.001_bib0175) 2003; 116 Matrisciano (10.1016/j.bbr.2014.12.001_bib0265) 2012; 4 Mesquita (10.1016/j.bbr.2014.12.001_bib0025) 2009; 14 Levenson (10.1016/j.bbr.2014.12.001_bib0115) 2005; 1 Fortress (10.1016/j.bbr.2014.12.001_bib0145) 2014; 35 Fride (10.1016/j.bbr.2014.12.001_bib0040) 1984; 17 Zhao (10.1016/j.bbr.2014.12.001_bib0170) 2010; 107 Entringer (10.1016/j.bbr.2014.12.001_bib0045) 2011; 108 Robertson (10.1016/j.bbr.2014.12.001_bib0210) 1999; 27 Wu (10.1016/j.bbr.2014.12.001_bib0245) 2007; 1141 Szuran (10.1016/j.bbr.2014.12.001_bib0070) 2000; 71 Sweatt (10.1016/j.bbr.2014.12.001_bib0135) 2009; 65 De Quervain (10.1016/j.bbr.2014.12.001_bib0090) 1998; 394 Stefanko (10.1016/j.bbr.2014.12.001_bib0165) 2009; 106 Fuks (10.1016/j.bbr.2014.12.001_bib0215) 2000; 24 Biala (10.1016/j.bbr.2014.12.001_bib0285) 2011; 21 Malaspina (10.1016/j.bbr.2014.12.001_bib0315) 2008; 8 Fride (10.1016/j.bbr.2014.12.001_bib0085) 1985; 22 Sierksma (10.1016/j.bbr.2014.12.001_bib0250) 2013; 34 Mychasiuk (10.1016/j.bbr.2014.12.001_bib0290) 2011; 180 Morgan (10.1016/j.bbr.2014.12.001_bib0310) 2011; 31 Matrisciano (10.1016/j.bbr.2014.12.001_bib0270) 2012; 68 Bowman (10.1016/j.bbr.2014.12.001_bib0030) 2004; 45 Wood (10.1016/j.bbr.2014.12.001_bib0130) 2006; 13 Dunn (10.1016/j.bbr.2014.12.001_sbref0200b) 2011; 59 Levenson (10.1016/j.bbr.2014.12.001_bib0110) 2004; 279 Markham (10.1016/j.bbr.2014.12.001_bib0060) 2010; 25 Braastad (10.1016/j.bbr.2014.12.001_bib0010) 1998; 61 Li (10.1016/j.bbr.2014.12.001_bib0190) 1993; 366 Wellberg (10.1016/j.bbr.2014.12.001_bib0305) 2001; 104 Jacobson (10.1016/j.bbr.2014.12.001_bib0275) 2007; 1 Cai (10.1016/j.bbr.2014.12.001_bib0100) 2007; 25 Moser (10.1016/j.bbr.2014.12.001_bib0235) 1998; 8 Vallee (10.1016/j.bbr.2014.12.001_bib0020) 1999; 11 Son (10.1016/j.bbr.2014.12.001_bib0095) 2006; 26 Levenson (10.1016/j.bbr.2014.12.001_bib0120) 2006; 63 Yang (10.1016/j.bbr.2014.12.001_bib0240) 2006; 16 Jensen Peña (10.1016/j.bbr.2014.12.001_bib0260) 2012; 6 Colvis (10.1016/j.bbr.2014.12.001_bib0140) 2005; 24 Day (10.1016/j.bbr.2014.12.001_sbref0200a) 2010; 13 Lemaire (10.1016/j.bbr.2014.12.001_bib0105) 2000; 97 Winston (10.1016/j.bbr.2014.12.001_bib0255) 2014; 5 Vallee (10.1016/j.bbr.2014.12.001_bib0050) 1997; 17 Levenson (10.1016/j.bbr.2014.12.001_bib0205) 2006; 281 Lehmann (10.1016/j.bbr.2014.12.001_bib0055) 2000; 107 Mychasiuk (10.1016/j.bbr.2014.12.001_bib0280) 2011; 33 Hawk (10.1016/j.bbr.2014.12.001_bib0160) 2011; 18 Salomon (10.1016/j.bbr.2014.12.001_bib0065) 2011; 23 Matthews (10.1016/j.bbr.2014.12.001_bib0300) 2002; 13 Morris (10.1016/j.bbr.2014.12.001_bib0220) 1982; 297 Miller (10.1016/j.bbr.2014.12.001_bib0125) 2008; 89 Darnaudery (10.1016/j.bbr.2014.12.001_bib0080) 2008; 57 Schenk (10.1016/j.bbr.2014.12.001_bib0225) 1985; 58 Guan (10.1016/j.bbr.2014.12.001_bib0150) 2009; 459 Chen (10.1016/j.bbr.2014.12.001_bib0195) 1998; 395 Markowska (10.1016/j.bbr.2014.12.001_bib0230) 1993; 107 Cabrera (10.1016/j.bbr.2014.12.001_bib0015) 1999; 32 Kofman (10.1016/j.bbr.2014.12.001_bib0005) 2002; 26 Li (10.1016/j.bbr.2014.12.001_bib0185) 1992; 69 Nan (10.1016/j.bbr.2014.12.001_bib0180) 1998; 393 Mychasiuk (10.1016/j.bbr.2014.12.001_bib0295) 2013; 241 Kay (10.1016/j.bbr.2014.12.001_bib0035) 1998; 63 Gue (10.1016/j.bbr.2014.12.001_bib0075) 2004; 150
References_xml	– volume: 107 start-page: 133 year: 2000 end-page: 144 ident: bib0055 article-title: Long-term effects of prenatal stress experience and postnatal maternal separation on emotionality and attentional processes publication-title: Behav Brain Res – volume: 13 start-page: 373 year: 2002 end-page: 380 ident: bib0300 article-title: Early programming of the hypothalamo-pituitary-adrenal axis publication-title: Trends Endocrinol Metab – volume: 297 start-page: 681 year: 1982 end-page: 683 ident: bib0220 article-title: Place navigation impaired in rats with hippocampal lesions publication-title: Nature – volume: 65 start-page: 191 year: 2009 end-page: 197 ident: bib0135 article-title: Experience-dependent epigenetic modifications in the central nervous system publication-title: Biol Psychiatry – volume: 393 start-page: 386 year: 1998 end-page: 390 ident: bib0180 article-title: Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex publication-title: Nature – volume: 281 start-page: 15763 year: 2006 end-page: 15773 ident: bib0205 article-title: Evidence that DNA (Cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus publication-title: J Biol Chem – volume: 27 start-page: 2291 year: 1999 end-page: 2298 ident: bib0210 article-title: The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors publication-title: Nucleic Acids Res – volume: 24 start-page: 10379 year: 2005 end-page: 10389 ident: bib0140 article-title: Epigenetic networks and gene regulation in the nervous system publication-title: J Neurosci – volume: 13 start-page: 1319 year: 2010 end-page: 1323 ident: bib0200 article-title: DNA methylation and memory formation publication-title: Nat Neurosci – volume: 89 start-page: 599 year: 2008 end-page: 603 ident: bib0125 article-title: DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity publication-title: Neurobiol Learn Mem – volume: 394 start-page: 787 year: 1998 end-page: 790 ident: bib0090 article-title: Stress and glucocorticoids impair retrieval of long-term spatial memory publication-title: Nature – volume: 57 start-page: 571 year: 2008 end-page: 585 ident: bib0080 article-title: Epigenetic programming of the stress response in male and female rats by prenatal restraint stress publication-title: Brain Res Rev – volume: 366 start-page: 362 year: 1993 end-page: 367 ident: bib0190 article-title: Role for DNA methylation in genomic imprinting publication-title: Nature – volume: 71 start-page: 353 year: 2000 end-page: 362 ident: bib0070 article-title: Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance publication-title: Physiol Behav – volume: 17 start-page: 651 year: 1984 end-page: 660 ident: bib0040 article-title: The effects of prenatal exposure to predictable or unpredictable stress on early development in the rat publication-title: Dev Psychobiol – volume: 25 start-page: 207 year: 2007 end-page: 213 ident: bib0100 article-title: Sex and region difference of the expression of ERK in prenatal stress hippocampus publication-title: Int J Dev Neurosci – volume: 68 start-page: 184 year: 2012 end-page: 194 ident: bib0270 article-title: Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice publication-title: Neuropharmacology – volume: 63 start-page: 397 year: 1998 end-page: 402 ident: bib0035 article-title: Prenatal stress depresses immune function in rats publication-title: Physiol Behav – volume: 1141 start-page: 205 year: 2007 end-page: 213 ident: bib0245 article-title: Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats publication-title: Brain Res – volume: 8 start-page: 1 year: 2008 end-page: 9 ident: bib0315 article-title: Acute maternal stress in pregnancy and schizophrenia in offspring: a cohort prospective study publication-title: BMC Psychiatry – volume: 45 start-page: 3778 year: 2004 end-page: 3787 ident: bib0030 article-title: Sexually dimorphic effects of stress on cognition, hormonal responses and central neurotransmitters publication-title: Endocrinology – volume: 241 start-page: 100 year: 2013 end-page: 105 ident: bib0295 article-title: Paternal stress prior to conception alters DNA methylation and behaviour of developing rat offspring publication-title: Neuroscience – volume: 34 start-page: 319 year: 2013 end-page: 337 ident: bib0250 article-title: Behavioural and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice publication-title: Neurobiol Aging – volume: 6 start-page: 39791 year: 2012 end-page: 39799 ident: bib0260 article-title: Epigenetic effects of prenatal stress on 11β-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain publication-title: PLoS One – volume: 17 start-page: 2626 year: 1997 end-page: 2636 ident: bib0050 article-title: Prenatal stress induces high anxiety and postnatal handling induces low handling in adult offspring: correlation with stress-induced corticosterone secretion publication-title: J Neurosci – volume: 150 start-page: 149 year: 2004 end-page: 157 ident: bib0075 article-title: Sex differences in learning deficits induced by prenatal stress in juvenile rats publication-title: Behav Brain Res – volume: 23 start-page: 118 year: 2011 end-page: 128 ident: bib0065 article-title: Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats publication-title: J Neuroendocrinol – volume: 116 start-page: 4905 year: 2003 end-page: 4916 ident: bib0175 article-title: Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons publication-title: J Cell Sci – volume: 69 start-page: 915 year: 1992 end-page: 926 ident: bib0185 article-title: Targeted mutation of the DNA methyltransferase gene results in embryonic lethality publication-title: Cell – volume: 25 start-page: 173 year: 2010 end-page: 176 ident: bib0060 article-title: Characterization of the cognitive impairments induced by prenatal exposure to stress in the rat publication-title: Front Behav Neurosci – volume: 1 start-page: 108 year: 2005 end-page: 118 ident: bib0115 article-title: Epigenetic mechanisms in memory formation publication-title: Nature – volume: 16 start-page: 431 year: 2006 end-page: 436 ident: bib0240 article-title: Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring publication-title: Hippocampus – volume: 279 start-page: 40545 year: 2004 end-page: 40559 ident: bib0110 article-title: Regulation of histone acetylation during memory formation in the hippocampus publication-title: J Biol Chem – volume: 35 start-page: 530 year: 2014 end-page: 549 ident: bib0145 article-title: Epigenetic regulation of estrogen-dependent memory publication-title: Front Neuroendocrinol – volume: 108 start-page: 513 year: 2011 end-page: 518 ident: bib0045 article-title: Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood publication-title: Proc Natl Acad Sci USA – volume: 104 start-page: 71 year: 2001 end-page: 79 ident: bib0305 article-title: Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour publication-title: Neuroscience – volume: 18 start-page: 367 year: 2011 end-page: 370 ident: bib0160 article-title: Post-training intrahippocampal inhibition of class I histone deacetylases enhances long-term object-location memory publication-title: Learn Mem – volume: 32 start-page: 1229 year: 1999 end-page: 1237 ident: bib0015 article-title: Effects of prenatal exposure to a mild chronic variable stress on body weight, preweaning mortality and rat behaviour publication-title: Braz J Med Biol Res – volume: 1 start-page: 171 year: 2007 end-page: 213 ident: bib0275 article-title: Feeling strained? Influence of genetic background on depression-related behavior in mice: a review publication-title: Behav Genet – volume: 18 start-page: 71 year: 2011 end-page: 79 ident: bib0155 article-title: HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner publication-title: Learn Mem – volume: 180 start-page: 105 year: 2011 end-page: 110 ident: bib0290 article-title: Intensity matters: brain, behaviour and the epigenome of prenatally stressed rats publication-title: Neuroscience – volume: 106 start-page: 9447 year: 2009 end-page: 9452 ident: bib0165 article-title: Modulation of long-term memory for object recognition via HDAC inhibition publication-title: Proc Natl Acad Sci USA – volume: 22 start-page: 2103 year: 1985 end-page: 2109 ident: bib0085 article-title: Prenatal stress impairs maternal behaviour in a conflict situation and reduces hippocampal benzodiazepine receptors publication-title: Life Sci – volume: 11 start-page: 2906 year: 1999 end-page: 2916 ident: bib0020 article-title: Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat publication-title: Eur J Neurosci – volume: 24 start-page: 88 year: 2000 end-page: 93 ident: bib0215 article-title: DNA methyltransferase Dnmt1 associates with histone deacetylase activity publication-title: Nature – volume: 33 start-page: 531 year: 2011 end-page: 538 ident: bib0280 article-title: Prenatal stress produces sexually dimorphic and regionally specific changes in gene expression in hippocampus and frontal cortex of developing rat offspring publication-title: Dev Neurosci – volume: 8 start-page: 608 year: 1998 end-page: 619 ident: bib0235 article-title: Functional differentiation in the hippocampus publication-title: Hippocampus – volume: 395 start-page: 89 year: 1998 end-page: 95 ident: bib0195 article-title: DNA hypomethylation leads to elevated mutation rates publication-title: Nature – volume: 58 start-page: 11 year: 1985 end-page: 28 ident: bib0225 article-title: Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions publication-title: Exp Brain Res – volume: 5 start-page: 715 year: 2014 end-page: 730 ident: bib0255 article-title: Chronic prenatal stress epigenetically modifies spinal cord BDNF expression to induce sex-specific visceral hypersensitivity in offspring publication-title: Neurogastroenterol Motil – volume: 13 start-page: 241 year: 2006 end-page: 244 ident: bib0130 article-title: Combinatorial chromatin modifications and memory storage: a code for memory publication-title: Learn Mem – volume: 107 start-page: 5605 year: 2010 end-page: 5610 ident: bib0170 article-title: Epigenetic alterations regulate the estradiol-induced enhancement of memory consolidation publication-title: Proc Natl Acad Sci – volume: 26 start-page: 3309 year: 2006 end-page: 3318 ident: bib0095 article-title: Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity publication-title: J Neurosci – volume: 31 start-page: 11748 year: 2011 end-page: 11755 ident: bib0310 article-title: Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage publication-title: J Neurosci – volume: 459 start-page: 55 year: 2009 end-page: 60 ident: bib0150 article-title: HDAC2 negatively regulates memory formation and synaptic plasticity publication-title: Nature – volume: 107 start-page: 627 year: 1993 end-page: 632 ident: bib0230 article-title: Variable-interval probe test as a tool for repeated measurements of spatial memory in the water maze publication-title: Behav Neurosci – volume: 26 start-page: 457 year: 2002 end-page: 470 ident: bib0005 article-title: The role of prenatal stress in the etiology of developmental behavioural disorders publication-title: Neurosci Behav Rev – volume: 14 start-page: 130 year: 2009 end-page: 135 ident: bib0025 article-title: Glucocorticoids and neuro- and behavioural development publication-title: Semin Fetal Neonatal Med – volume: 61 start-page: 159 year: 1998 end-page: 180 ident: bib0010 article-title: Effects of prenatal stress on behaviour of offspring of laboratory and farmed animals publication-title: Appl Anim Behav Sci – volume: 21 start-page: 1114 year: 2011 end-page: 1125 ident: bib0285 article-title: Prenatal stress diminishes gender differences in behavior and in expression of hippocampal synaptic genes and proteins in rats publication-title: Hippocampus – volume: 97 start-page: 11032 year: 2000 end-page: 11037 ident: bib0105 article-title: Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus publication-title: PNAS – volume: 63 start-page: 1009 year: 2006 end-page: 1016 ident: bib0120 article-title: Epigenetic mechanisms: a common theme in vertebrate and invertebrate memory formation publication-title: Cell Mol Life Sci – volume: 4 start-page: 929 year: 2012 end-page: 938 ident: bib0265 article-title: Pharmacological activation of group-II metabotropic glutamate receptors corrects a schizophrenia-like phenotype induced by prenatal stress in mice publication-title: Neuropsychopharmacology – volume: 63 start-page: 1009 year: 2006 ident: 10.1016/j.bbr.2014.12.001_bib0120 article-title: Epigenetic mechanisms: a common theme in vertebrate and invertebrate memory formation publication-title: Cell Mol Life Sci doi: 10.1007/s00018-006-6026-6 – volume: 13 start-page: 241 year: 2006 ident: 10.1016/j.bbr.2014.12.001_bib0130 article-title: Combinatorial chromatin modifications and memory storage: a code for memory publication-title: Learn Mem doi: 10.1101/lm.278206 – volume: 18 start-page: 367 year: 2011 ident: 10.1016/j.bbr.2014.12.001_bib0160 article-title: Post-training intrahippocampal inhibition of class I histone deacetylases enhances long-term object-location memory publication-title: Learn Mem doi: 10.1101/lm.2097411 – volume: 150 start-page: 149 year: 2004 ident: 10.1016/j.bbr.2014.12.001_bib0075 article-title: Sex differences in learning deficits induced by prenatal stress in juvenile rats publication-title: Behav Brain Res doi: 10.1016/S0166-4328(03)00250-X – volume: 395 start-page: 89 year: 1998 ident: 10.1016/j.bbr.2014.12.001_bib0195 article-title: DNA hypomethylation leads to elevated mutation rates publication-title: Nature doi: 10.1038/25779 – volume: 34 start-page: 319 year: 2013 ident: 10.1016/j.bbr.2014.12.001_bib0250 article-title: Behavioural and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice publication-title: Neurobiol Aging doi: 10.1016/j.neurobiolaging.2012.05.012 – volume: 297 start-page: 681 year: 1982 ident: 10.1016/j.bbr.2014.12.001_bib0220 article-title: Place navigation impaired in rats with hippocampal lesions publication-title: Nature doi: 10.1038/297681a0 – volume: 17 start-page: 651 year: 1984 ident: 10.1016/j.bbr.2014.12.001_bib0040 article-title: The effects of prenatal exposure to predictable or unpredictable stress on early development in the rat publication-title: Dev Psychobiol doi: 10.1002/dev.420170607 – volume: 59 start-page: 290 year: 2011 ident: 10.1016/j.bbr.2014.12.001_sbref0200b article-title: Sex-specificity in transgenerational epigenetic programming publication-title: Horm Behav doi: 10.1016/j.yhbeh.2010.05.004 – volume: 116 start-page: 4905 year: 2003 ident: 10.1016/j.bbr.2014.12.001_bib0175 article-title: Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons publication-title: J Cell Sci doi: 10.1242/jcs.00804 – volume: 5 start-page: 715 year: 2014 ident: 10.1016/j.bbr.2014.12.001_bib0255 article-title: Chronic prenatal stress epigenetically modifies spinal cord BDNF expression to induce sex-specific visceral hypersensitivity in offspring publication-title: Neurogastroenterol Motil doi: 10.1111/nmo.12326 – volume: 25 start-page: 207 year: 2007 ident: 10.1016/j.bbr.2014.12.001_bib0100 article-title: Sex and region difference of the expression of ERK in prenatal stress hippocampus publication-title: Int J Dev Neurosci doi: 10.1016/j.ijdevneu.2007.03.009 – volume: 281 start-page: 15763 year: 2006 ident: 10.1016/j.bbr.2014.12.001_bib0205 article-title: Evidence that DNA (Cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus publication-title: J Biol Chem doi: 10.1074/jbc.M511767200 – volume: 68 start-page: 184 year: 2012 ident: 10.1016/j.bbr.2014.12.001_bib0270 article-title: Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice publication-title: Neuropharmacology doi: 10.1016/j.neuropharm.2012.04.013 – volume: 58 start-page: 11 year: 1985 ident: 10.1016/j.bbr.2014.12.001_bib0225 article-title: Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions publication-title: Exp Brain Res doi: 10.1007/BF00238949 – volume: 89 start-page: 599 year: 2008 ident: 10.1016/j.bbr.2014.12.001_bib0125 article-title: DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity publication-title: Neurobiol Learn Mem doi: 10.1016/j.nlm.2007.07.016 – volume: 6 start-page: 39791 year: 2012 ident: 10.1016/j.bbr.2014.12.001_bib0260 article-title: Epigenetic effects of prenatal stress on 11β-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain publication-title: PLoS One doi: 10.1371/journal.pone.0039791 – volume: 27 start-page: 2291 year: 1999 ident: 10.1016/j.bbr.2014.12.001_bib0210 article-title: The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors publication-title: Nucleic Acids Res doi: 10.1093/nar/27.11.2291 – volume: 8 start-page: 608 year: 1998 ident: 10.1016/j.bbr.2014.12.001_bib0235 article-title: Functional differentiation in the hippocampus publication-title: Hippocampus doi: 10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7 – volume: 108 start-page: 513 year: 2011 ident: 10.1016/j.bbr.2014.12.001_bib0045 article-title: Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.1107759108 – volume: 24 start-page: 10379 year: 2005 ident: 10.1016/j.bbr.2014.12.001_bib0140 article-title: Epigenetic networks and gene regulation in the nervous system publication-title: J Neurosci doi: 10.1523/JNEUROSCI.4119-05.2005 – volume: 97 start-page: 11032 year: 2000 ident: 10.1016/j.bbr.2014.12.001_bib0105 article-title: Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus publication-title: PNAS doi: 10.1073/pnas.97.20.11032 – volume: 33 start-page: 531 year: 2011 ident: 10.1016/j.bbr.2014.12.001_bib0280 article-title: Prenatal stress produces sexually dimorphic and regionally specific changes in gene expression in hippocampus and frontal cortex of developing rat offspring publication-title: Dev Neurosci doi: 10.1159/000335524 – volume: 459 start-page: 55 year: 2009 ident: 10.1016/j.bbr.2014.12.001_bib0150 article-title: HDAC2 negatively regulates memory formation and synaptic plasticity publication-title: Nature doi: 10.1038/nature07925 – volume: 1141 start-page: 205 year: 2007 ident: 10.1016/j.bbr.2014.12.001_bib0245 article-title: Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats publication-title: Brain Res doi: 10.1016/j.brainres.2007.01.024 – volume: 241 start-page: 100 year: 2013 ident: 10.1016/j.bbr.2014.12.001_bib0295 article-title: Paternal stress prior to conception alters DNA methylation and behaviour of developing rat offspring publication-title: Neuroscience doi: 10.1016/j.neuroscience.2013.03.025 – volume: 8 start-page: 1 year: 2008 ident: 10.1016/j.bbr.2014.12.001_bib0315 article-title: Acute maternal stress in pregnancy and schizophrenia in offspring: a cohort prospective study publication-title: BMC Psychiatry doi: 10.1186/1471-244X-8-71 – volume: 35 start-page: 530 year: 2014 ident: 10.1016/j.bbr.2014.12.001_bib0145 article-title: Epigenetic regulation of estrogen-dependent memory publication-title: Front Neuroendocrinol doi: 10.1016/j.yfrne.2014.05.001 – volume: 180 start-page: 105 year: 2011 ident: 10.1016/j.bbr.2014.12.001_bib0290 article-title: Intensity matters: brain, behaviour and the epigenome of prenatally stressed rats publication-title: Neuroscience doi: 10.1016/j.neuroscience.2011.02.026 – volume: 393 start-page: 386 year: 1998 ident: 10.1016/j.bbr.2014.12.001_bib0180 article-title: Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex publication-title: Nature doi: 10.1038/30764 – volume: 63 start-page: 397 year: 1998 ident: 10.1016/j.bbr.2014.12.001_bib0035 article-title: Prenatal stress depresses immune function in rats publication-title: Physiol Behav doi: 10.1016/S0031-9384(97)00456-3 – volume: 26 start-page: 3309 year: 2006 ident: 10.1016/j.bbr.2014.12.001_bib0095 article-title: Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity publication-title: J Neurosci doi: 10.1523/JNEUROSCI.3850-05.2006 – volume: 23 start-page: 118 year: 2011 ident: 10.1016/j.bbr.2014.12.001_bib0065 article-title: Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats publication-title: J Neuroendocrinol doi: 10.1111/j.1365-2826.2010.02097.x – volume: 45 start-page: 3778 year: 2004 ident: 10.1016/j.bbr.2014.12.001_bib0030 article-title: Sexually dimorphic effects of stress on cognition, hormonal responses and central neurotransmitters publication-title: Endocrinology doi: 10.1210/en.2003-1759 – volume: 32 start-page: 1229 year: 1999 ident: 10.1016/j.bbr.2014.12.001_bib0015 article-title: Effects of prenatal exposure to a mild chronic variable stress on body weight, preweaning mortality and rat behaviour publication-title: Braz J Med Biol Res doi: 10.1590/S0100-879X1999001000009 – volume: 21 start-page: 1114 year: 2011 ident: 10.1016/j.bbr.2014.12.001_bib0285 article-title: Prenatal stress diminishes gender differences in behavior and in expression of hippocampal synaptic genes and proteins in rats publication-title: Hippocampus doi: 10.1002/hipo.20825 – volume: 14 start-page: 130 year: 2009 ident: 10.1016/j.bbr.2014.12.001_bib0025 article-title: Glucocorticoids and neuro- and behavioural development publication-title: Semin Fetal Neonatal Med doi: 10.1016/j.siny.2008.11.002 – volume: 71 start-page: 353 year: 2000 ident: 10.1016/j.bbr.2014.12.001_bib0070 article-title: Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance publication-title: Physiol Behav doi: 10.1016/S0031-9384(00)00351-6 – volume: 57 start-page: 571 year: 2008 ident: 10.1016/j.bbr.2014.12.001_bib0080 article-title: Epigenetic programming of the stress response in male and female rats by prenatal restraint stress publication-title: Brain Res Rev doi: 10.1016/j.brainresrev.2007.11.004 – volume: 24 start-page: 88 year: 2000 ident: 10.1016/j.bbr.2014.12.001_bib0215 article-title: DNA methyltransferase Dnmt1 associates with histone deacetylase activity publication-title: Nature – volume: 26 start-page: 457 year: 2002 ident: 10.1016/j.bbr.2014.12.001_bib0005 article-title: The role of prenatal stress in the etiology of developmental behavioural disorders publication-title: Neurosci Behav Rev doi: 10.1016/S0149-7634(02)00015-5 – volume: 106 start-page: 9447 year: 2009 ident: 10.1016/j.bbr.2014.12.001_bib0165 article-title: Modulation of long-term memory for object recognition via HDAC inhibition publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.0903964106 – volume: 65 start-page: 191 year: 2009 ident: 10.1016/j.bbr.2014.12.001_bib0135 article-title: Experience-dependent epigenetic modifications in the central nervous system publication-title: Biol Psychiatry doi: 10.1016/j.biopsych.2008.09.002 – volume: 394 start-page: 787 year: 1998 ident: 10.1016/j.bbr.2014.12.001_bib0090 article-title: Stress and glucocorticoids impair retrieval of long-term spatial memory publication-title: Nature doi: 10.1038/29542 – volume: 107 start-page: 133 year: 2000 ident: 10.1016/j.bbr.2014.12.001_bib0055 article-title: Long-term effects of prenatal stress experience and postnatal maternal separation on emotionality and attentional processes publication-title: Behav Brain Res doi: 10.1016/S0166-4328(99)00122-9 – volume: 366 start-page: 362 year: 1993 ident: 10.1016/j.bbr.2014.12.001_bib0190 article-title: Role for DNA methylation in genomic imprinting publication-title: Nature doi: 10.1038/366362a0 – volume: 1 start-page: 171 year: 2007 ident: 10.1016/j.bbr.2014.12.001_bib0275 article-title: Feeling strained? Influence of genetic background on depression-related behavior in mice: a review publication-title: Behav Genet doi: 10.1007/s10519-006-9106-3 – volume: 61 start-page: 159 year: 1998 ident: 10.1016/j.bbr.2014.12.001_bib0010 article-title: Effects of prenatal stress on behaviour of offspring of laboratory and farmed animals publication-title: Appl Anim Behav Sci doi: 10.1016/S0168-1591(98)00188-9 – volume: 107 start-page: 5605 year: 2010 ident: 10.1016/j.bbr.2014.12.001_bib0170 article-title: Epigenetic alterations regulate the estradiol-induced enhancement of memory consolidation publication-title: Proc Natl Acad Sci doi: 10.1073/pnas.0910578107 – volume: 31 start-page: 11748 year: 2011 ident: 10.1016/j.bbr.2014.12.001_bib0310 article-title: Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage publication-title: J Neurosci doi: 10.1523/JNEUROSCI.1887-11.2011 – volume: 22 start-page: 2103 year: 1985 ident: 10.1016/j.bbr.2014.12.001_bib0085 article-title: Prenatal stress impairs maternal behaviour in a conflict situation and reduces hippocampal benzodiazepine receptors publication-title: Life Sci doi: 10.1016/0024-3205(85)90306-6 – volume: 18 start-page: 71 year: 2011 ident: 10.1016/j.bbr.2014.12.001_bib0155 article-title: HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner publication-title: Learn Mem doi: 10.1101/lm.1986911 – volume: 69 start-page: 915 year: 1992 ident: 10.1016/j.bbr.2014.12.001_bib0185 article-title: Targeted mutation of the DNA methyltransferase gene results in embryonic lethality publication-title: Cell doi: 10.1016/0092-8674(92)90611-F – volume: 17 start-page: 2626 year: 1997 ident: 10.1016/j.bbr.2014.12.001_bib0050 article-title: Prenatal stress induces high anxiety and postnatal handling induces low handling in adult offspring: correlation with stress-induced corticosterone secretion publication-title: J Neurosci doi: 10.1523/JNEUROSCI.17-07-02626.1997 – volume: 107 start-page: 627 year: 1993 ident: 10.1016/j.bbr.2014.12.001_bib0230 article-title: Variable-interval probe test as a tool for repeated measurements of spatial memory in the water maze publication-title: Behav Neurosci doi: 10.1037/0735-7044.107.4.627 – volume: 279 start-page: 40545 year: 2004 ident: 10.1016/j.bbr.2014.12.001_bib0110 article-title: Regulation of histone acetylation during memory formation in the hippocampus publication-title: J Biol Chem doi: 10.1074/jbc.M402229200 – volume: 4 start-page: 929 year: 2012 ident: 10.1016/j.bbr.2014.12.001_bib0265 article-title: Pharmacological activation of group-II metabotropic glutamate receptors corrects a schizophrenia-like phenotype induced by prenatal stress in mice publication-title: Neuropsychopharmacology doi: 10.1038/npp.2011.274 – volume: 16 start-page: 431 year: 2006 ident: 10.1016/j.bbr.2014.12.001_bib0240 article-title: Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring publication-title: Hippocampus doi: 10.1002/hipo.20181 – volume: 11 start-page: 2906 year: 1999 ident: 10.1016/j.bbr.2014.12.001_bib0020 article-title: Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat publication-title: Eur J Neurosci doi: 10.1046/j.1460-9568.1999.00705.x – volume: 104 start-page: 71 year: 2001 ident: 10.1016/j.bbr.2014.12.001_bib0305 article-title: Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour publication-title: Neuroscience doi: 10.1016/S0306-4522(01)00065-3 – volume: 13 start-page: 1319 year: 2010 ident: 10.1016/j.bbr.2014.12.001_sbref0200a article-title: DNA methylation and memory formation publication-title: Nat Neurosci doi: 10.1038/nn.2666 – volume: 13 start-page: 373 year: 2002 ident: 10.1016/j.bbr.2014.12.001_bib0300 article-title: Early programming of the hypothalamo-pituitary-adrenal axis publication-title: Trends Endocrinol Metab doi: 10.1016/S1043-2760(02)00690-2 – volume: 25 start-page: 173 year: 2010 ident: 10.1016/j.bbr.2014.12.001_bib0060 article-title: Characterization of the cognitive impairments induced by prenatal exposure to stress in the rat publication-title: Front Behav Neurosci – volume: 1 start-page: 108 year: 2005 ident: 10.1016/j.bbr.2014.12.001_bib0115 article-title: Epigenetic mechanisms in memory formation publication-title: Nature
SSID	ssj0004051
Score	2.4365332
Snippet	•Effects of chronic unpredictable prenatal stress were tested in adult offspring.•Prenatal stress impaired spatial memory in adult male and female... Stress during pregnancy has a wide variety of negative effects in both human [1] and animal offspring [2]. These effects are especially apparent in various...
SourceID	pubmedcentral proquest pubmed crossref elsevier
SourceType	Open Access Repository Aggregation Database Index Database Enrichment Source Publisher
StartPage	1
SubjectTerms	Acetylation Animals Chronic unpredictable stress Corticosterone - blood DNA (Cytosine-5-)-Methyltransferase 1 DNA (Cytosine-5-)-Methyltransferases - genetics DNA methyltransferase Epigenesis, Genetic Female Gene Expression Heterochromatin - metabolism Hippocampus - metabolism Histone acetylation Histones - genetics Male Maze Learning Memory Disorders Mice Mice, Inbred C57BL Morris water maze Mouse Pregnancy Prenatal Exposure Delayed Effects - genetics Prenatal Exposure Delayed Effects - psychology Risk Factors Sex differences Sex Factors Spatial Memory Stress, Psychological - blood Stress, Psychological - complications Stress, Psychological - genetics Stress, Psychological - psychology
Title	Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression
URI	https://dx.doi.org/10.1016/j.bbr.2014.12.001 https://www.ncbi.nlm.nih.gov/pubmed/25496779 https://www.proquest.com/docview/1652431955 https://www.proquest.com/docview/1673381303 https://pubmed.ncbi.nlm.nih.gov/PMC4305490
Volume	281
WOSCitedRecordID	wos000349504600001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText	1
inHoldings	1
isFullTextHit
isPrint
journalDatabaseRights	– providerCode: PRVESC databaseName: Elsevier SD Freedom Collection Journals 2021 customDbUrl: eissn: 1872-7549 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0004051 issn: 0166-4328 databaseCode: AIEXJ dateStart: 19950123 isFulltext: true titleUrlDefault: https://www.sciencedirect.com providerName: Elsevier
link	http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1bb9MwFLa6jQdeEDAu5TIZCfFAlSmO4zh5LGOIizb1YUh9i5LYVbOtSZRetP0Y_gC_kuNLkrZABUhIVVQlsRPpfLHP9TsIvU5oFkQ-TRw3nYCBwknkRFRGDieChQlJiaRCN5vg5-fheByNer3vTS3M6poXRXhzE1X_VdRwDoStSmf_QtztpHAC_oPQ4Qhih-MfCX5Uy0K3BLFlIGB0L1Xa1VzlTutakZmKqwupuCMWhqJZVoqUU9Uz2krgeZP_OM2rCra7WbXUM2kP30oaFRNEUmbTulRKb9GVQZqUdUUJC8qsmla1ETDptsVGDNkwBGjej1R1qhhY5qHWQ_1OFmW-sMm8uRy8P-7CUld5ZjTg-VXZgrC2feG_JPVtMTg7XvdpEKaSukxVZ-PmDALHp7ZsXJqlOeRgCzBDcGqXW7K-b_9yQzC-icvjNFXkr8TXvl_jPlnDQjXTYFDGcsBNc5stFu7R2YkiR_Mjdw8deJxFsIIeDD-djj93VbguM90v7bs3MXSdTbj1fMVBbR_2O4XoZ4NnO293TRG6uI_uWQsGDw3yHqCeLB6iwyFgrpzd4jdY5xTrYM0h-taAERswYgtGbMGIDRhxA0YM0MEdGLEFIwzDAEa8BkbcgRGXE7wFRtyCUc9owYjVtLgD4yP09cPpxclHxzYEcTIwpBeOCDMygR3Rk0Qy4VIeEkWsLLyJGwqRBTSVPBPM5zxJuCcEJambJWHq-pJOQp_Rx2i_KAv5FOFIBDzx4QcasO9SEVEmUiIkAzOOJmzSR24jlTizbPmqact13KRFXsYg01jJNCaeSg3to7ftkMpQxey62W9EHVtd1-iwMSB317BXDSxi2AdUcC8pZLmcxyRgHhgDEWO77uEUNHTQWvvoiYFS-6YNHPuIb4CsvUHx0G9eKfKp5qO3H8azfx75HN3tVoEXaH9RL-VLdCdbLfJ5fYT2-Dg8sl_bD4XTDSU
linkProvider	Elsevier
openUrl	ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Prenatal+stress+induces+spatial+memory+deficits+and+epigenetic+changes+in+the+hippocampus+indicative+of+heterochromatin+formation+and+reduced+gene+expression&rft.jtitle=Behavioural+brain+research&rft.au=Benoit%2C+Jamie+D.&rft.au=Rakic%2C+Pasko&rft.au=Frick%2C+Karyn+M.&rft.date=2015-03-15&rft.issn=0166-4328&rft.eissn=1872-7549&rft.spage=1&rft.epage=8&rft_id=info:doi/10.1016%2Fj.bbr.2014.12.001&rft_id=info%3Apmid%2F25496779&rft.externalDocID=PMC4305490
thumbnail_l	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0166-4328&client=summon
thumbnail_m	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0166-4328&client=summon
thumbnail_s	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0166-4328&client=summon