Multi- and Transgenerational Outcomes of an Exposure to a Mixture of Endocrine-Disrupting Chemicals (EDCs) on Puberty and Maternal Behavior in the Female Rat.


Journal

Environmental health perspectives
ISSN: 1552-9924
Titre abrégé: Environ Health Perspect
Pays: United States
ID NLM: 0330411

Informations de publication

Date de publication:
08 2021
Historique:
entrez: 12 8 2021
pubmed: 13 8 2021
medline: 17 3 2022
Statut: ppublish

Résumé

The effects of endocrine-disrupting chemicals (EDCs) on fertility and reproductive development represent a rising concern in modern societies. Although the neuroendocrine control of sexual maturation is a major target of EDCs, little is known about the potential role of the hypothalamus in puberty and ovulation disruption transmitted across generations. We hypothesized that developmental exposure to an environmentally relevant dose of EDC mixture could induce multi- and/or transgenerational alterations of sexual maturation and maternal care in female rats through epigenetic reprograming of the hypothalamus. We investigated the transmission of a disrupted reproductive phenotype via the maternal germline or via nongenomic mechanisms involving maternal care. Adult female Wistar rats were exposed prior to and during gestation and until the end of lactation to a mixture of the following 13 EDCs: di- Germ cell (F2) and transgenerationally (F3) EDC-exposed females, but not F1, displayed delayed pubertal onset and altered folliculogenesis. We reported a transgenerational alteration of key hypothalamic genes controlling puberty and ovulation ( Rats developmentally exposed to an EDC mixture exhibited multi- and transgenerational disruption of sexual maturation and maternal care via hypothalamic epigenetic reprogramming. These results raise concerns about the impact of EDC mixtures on future generations. https://doi.org/10.1289/EHP8795.

Sections du résumé

BACKGROUND
The effects of endocrine-disrupting chemicals (EDCs) on fertility and reproductive development represent a rising concern in modern societies. Although the neuroendocrine control of sexual maturation is a major target of EDCs, little is known about the potential role of the hypothalamus in puberty and ovulation disruption transmitted across generations.
OBJECTIVES
We hypothesized that developmental exposure to an environmentally relevant dose of EDC mixture could induce multi- and/or transgenerational alterations of sexual maturation and maternal care in female rats through epigenetic reprograming of the hypothalamus. We investigated the transmission of a disrupted reproductive phenotype via the maternal germline or via nongenomic mechanisms involving maternal care.
METHODS
Adult female Wistar rats were exposed prior to and during gestation and until the end of lactation to a mixture of the following 13 EDCs: di-
RESULTS
Germ cell (F2) and transgenerationally (F3) EDC-exposed females, but not F1, displayed delayed pubertal onset and altered folliculogenesis. We reported a transgenerational alteration of key hypothalamic genes controlling puberty and ovulation (
DISCUSSION
Rats developmentally exposed to an EDC mixture exhibited multi- and transgenerational disruption of sexual maturation and maternal care via hypothalamic epigenetic reprogramming. These results raise concerns about the impact of EDC mixtures on future generations. https://doi.org/10.1289/EHP8795.

Identifiants

pubmed: 34383603
doi: 10.1289/EHP8795
pmc: PMC8360047
doi:

Substances chimiques

Endocrine Disruptors 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

87003

Subventions

Organisme : NIH HHS
ID : P51 OD011092
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD084542
Pays : United States

Commentaires et corrections

Type : CommentIn

Références

Toxicology. 2013 Dec 6;314(1):65-75
pubmed: 24056307
Ann Med. 2003;35(4):244-55
pubmed: 12846266
Biol Reprod. 1978 Oct;19(3):597-605
pubmed: 363183
Reprod Fertil Dev. 2020 Mar;32(6):610-618
pubmed: 32209209
Toxicol Sci. 2000 May;55(1):143-51
pubmed: 10788569
Endocrinology. 2017 Jun 1;158(6):1739-1754
pubmed: 28368545
Toxicol Sci. 1998 Oct;45(2):162-73
pubmed: 9848123
N Engl J Med. 2003 Oct 23;349(17):1614-27
pubmed: 14573733
Environ Int. 2017 Feb;99:177-184
pubmed: 27865524
Sci Rep. 2016 Jan 27;6:19789
pubmed: 26813099
Mol Cell Endocrinol. 2006 Jul 25;254-255:32-8
pubmed: 16781054
Biol Reprod. 2007 Oct;77(4):734-42
pubmed: 17596564
J Vet Med Sci. 2002 Mar;64(3):227-35
pubmed: 11999442
Front Neuroendocrinol. 2015 Jul;38:12-36
pubmed: 25592640
Biol Reprod. 2009 Oct;81(4):690-9
pubmed: 19535786
Endocrinology. 2017 Jun 1;158(6):1727-1738
pubmed: 28324068
In Vivo. 2005 May-Jun;19(3):487-94
pubmed: 15875766
Toxicology. 2019 Jun 1;421:30-40
pubmed: 30940548
Endocrinology. 2019 Nov 1;160(11):2558-2572
pubmed: 31503316
Neuroendocrinology. 2021;111(7):678-695
pubmed: 32575098
Biol Reprod. 2014 Jun;90(6):136
pubmed: 24804967
Endocrinology. 2015 Jul;156(7):2563-70
pubmed: 25853665
J Endocrinol. 2007 Jul;194(1):201-12
pubmed: 17592034
Reprod Toxicol. 2015 Jun;53:23-32
pubmed: 25765777
Reprod Toxicol. 2017 Dec;74:150-157
pubmed: 28970132
Endocrinology. 2013 May;154(5):1873-84
pubmed: 23525218
Regul Toxicol Pharmacol. 2011 Feb;59(1):91-100
pubmed: 20875480
Toxicol Sci. 2018 Jun 1;163(2):420-429
pubmed: 29471507
Neuron. 2006 Oct 19;52(2):271-80
pubmed: 17046690
Proc Natl Acad Sci U S A. 2015 Oct 20;112(42):13109-14
pubmed: 26443858
Life Sci. 2009 Nov 18;85(21-22):742-52
pubmed: 19837096
Neuroendocrinology. 1989 Apr;49(4):402-8
pubmed: 2541362
Reprod Toxicol. 2010 Dec;30(4):550-7
pubmed: 20692330
Mol Cell Endocrinol. 2010 Aug 5;324(1-2):45-50
pubmed: 20109523
Environ Health Perspect. 2007 Dec;115 Suppl 1:42-50
pubmed: 18174949
Trends Genet. 2013 Mar;29(3):176-86
pubmed: 23410786
PLoS One. 2018 Aug 29;13(8):e0202662
pubmed: 30157260
Exp Clin Endocrinol Diabetes. 2010 May;118(5):298-303
pubmed: 20198561
Toxicol Appl Pharmacol. 2019 Sep 15;379:114629
pubmed: 31211961
Brain Res Bull. 2005 Apr 15;65(3):255-60
pubmed: 15811589
Horm Behav. 2013 Nov;64(5):833-9
pubmed: 24100195
Iran J Basic Med Sci. 2018 Aug;21(8):848-855
pubmed: 30186573
Pediatrics. 2010 Sep;126(3):e583-90
pubmed: 20696727
Toxicol Lett. 2009 Aug 25;189(1):14-20
pubmed: 19410640
Nat Rev Endocrinol. 2021 Feb;17(2):83-96
pubmed: 33288917
Toxicol Appl Pharmacol. 2010 Sep 1;247(2):98-104
pubmed: 20621667
Environ Health Perspect. 2007 Jun;115(6):876-82
pubmed: 17589594
Environ Health Perspect. 2007 Dec;115 Suppl 1:98-105
pubmed: 18174957
Horm Behav. 2019 Jan;107:96-109
pubmed: 30576639
Reprod Toxicol. 2017 Mar;68:3-33
pubmed: 27760374
Neurotoxicology. 2019 Sep;74:139-148
pubmed: 31251963
Toxicol Appl Pharmacol. 2006 Jun 1;213(2):160-71
pubmed: 16375936
Reprod Toxicol. 2017 Sep;72:97-105
pubmed: 28526456
Endocrinology. 2018 Jan 1;159(1):132-144
pubmed: 29165653
Endocrinology. 2016 Oct;157(10):3856-3872
pubmed: 27571134
Toxicol Sci. 2006 Sep;93(1):164-71
pubmed: 16763069
Environ Health Perspect. 2013 Apr;121(4):A104-6
pubmed: 23548368
Toxicol Sci. 2010 Sep;117(1):54-62
pubmed: 20566471
Toxicol Appl Pharmacol. 2007 Jan 15;218(2):152-65
pubmed: 17188730
Birth Defects Res B Dev Reprod Toxicol. 2007 Apr;80(2):84-97
pubmed: 17342777
Environ Health Perspect. 2010 May;118(5):679-85
pubmed: 20056562
Environ Health Perspect. 2009 May;117(5):757-62
pubmed: 19479018
Int J Androl. 2012 Jun;35(3):303-16
pubmed: 22372636
Endocrinology. 2019 Jun 1;160(6):1421-1435
pubmed: 30998239
Endocr Rev. 2015 Dec;36(6):E1-E150
pubmed: 26544531
PLoS One. 2013;8(1):e55387
pubmed: 23359474
Reprod Toxicol. 2011 Apr;31(3):280-9
pubmed: 20951797
Mol Cell Endocrinol. 2011 Aug 6;342(1-2):8-19
pubmed: 21672609
Front Genet. 2015 Mar 02;6:56
pubmed: 25784924
Toxicol Lett. 2010 Dec 15;199(3):323-32
pubmed: 20920559
Neurotoxicology. 2009 Mar;30(2):249-60
pubmed: 19150460
Endocrinology. 2004 Jun;145(6):2775-83
pubmed: 14988382
Toxicol Sci. 2007 Dec;100(2):464-73
pubmed: 17785682
Environ Health Perspect. 2007 Dec;115 Suppl 1:122-8
pubmed: 18174960
Toxicol Sci. 2001 Aug;62(2):236-49
pubmed: 11452136
Sci Rep. 2014 May 02;4:4873
pubmed: 24786242
Environ Health Perspect. 2019 Oct;127(10):107011
pubmed: 31652106
New Dir Child Adolesc Dev. 2016 Sep;2016(153):9-21
pubmed: 27589495
Nat Rev Genet. 2007 Apr;8(4):253-62
pubmed: 17363974
Toxicol Sci. 2008 Sep;105(1):153-65
pubmed: 18411233
Toxicology. 2004 Dec 1;205(1-2):131-7
pubmed: 15458798
PLoS One. 2012;7(2):e31901
pubmed: 22389676
Clin Exp Reprod Med. 2011 Jun;38(2):75-81
pubmed: 22384422
Horm Behav. 2008 Jun;54(1):178-84
pubmed: 18417127
Toxicol Sci. 2008 Mar;102(1):33-41
pubmed: 18032409
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Science. 1997 Sep 12;277(5332):1659-62
pubmed: 9287218
Nucleic Acids Res. 2019 May 7;47(8):e47
pubmed: 30783653
Science. 1999 Nov 5;286(5442):1155-8
pubmed: 10550053
Nat Commun. 2018 Jan 4;9(1):57
pubmed: 29302059
Int J Androl. 2010 Apr;33(2):434-42
pubmed: 20487043
Reprod Toxicol. 2016 Apr;60:39-52
pubmed: 26746108
Environ Health Perspect. 2006 Dec;114(12):1843-6
pubmed: 17185273
Hum Reprod. 2012 Apr;27(4):1025-33
pubmed: 22267834
Reproduction. 2014 Mar 02;147(4):465-76
pubmed: 24287426
Reprod Toxicol. 2014 Apr;44:63-72
pubmed: 24316331
Endocrinology. 2012 Aug;153(8):3828-38
pubmed: 22707478
Acta Endocrinol (Copenh). 1969 Sep;62(1):98-116
pubmed: 5394354
Nucleic Acids Res. 2001 May 1;29(9):e45
pubmed: 11328886
Biol Reprod. 2012 Aug 02;87(2):28
pubmed: 22572997
Toxicol Appl Pharmacol. 2017 May 1;322:113-121
pubmed: 28286118
J Toxicol Sci. 2009;34 Suppl 1:SP111-9
pubmed: 19265277
Endocrinology. 2012 Nov;153(11):5587-99
pubmed: 22948210
Regul Pept. 2000 Aug 25;92(1-3):17-24
pubmed: 11024560
Nat Commun. 2018 Oct 10;9(1):4194
pubmed: 30305620
Ecotoxicol Environ Saf. 2020 Jul 15;198:110698
pubmed: 32388187
Nat Neurosci. 2004 Aug;7(8):847-54
pubmed: 15220929
Reprod Toxicol. 2011 Feb;31(2):177-83
pubmed: 21055461
Endocrinology. 1989 Aug;125(2):1090-6
pubmed: 2546737
Exp Clin Endocrinol Diabetes. 2008 Feb;116(2):94-8
pubmed: 18286425
Toxicol Appl Pharmacol. 2015 Dec 15;289(3):507-14
pubmed: 26493930
Reproduction. 2014 Mar 02;147(4):489-501
pubmed: 24298046
J Endocrinol. 2014 Apr 22;221(2):201-13
pubmed: 24532816
Endocrinology. 2014 Aug;155(8):2986-95
pubmed: 24905671
Neurotoxicol Teratol. 2014 Jan-Feb;41:16-26
pubmed: 24269606
Sci Total Environ. 2014 Oct 15;496:282-288
pubmed: 25089690
Reprod Toxicol. 2010 Dec;30(4):625-34
pubmed: 20951796
Reprod Toxicol. 2015 Jul;54:47-57
pubmed: 25305543
Toxicol Appl Pharmacol. 2015 May 1;284(3):354-62
pubmed: 25771130
Biol Reprod. 2019 Oct 25;101(4):854-867
pubmed: 31318015
Reprod Toxicol. 2009 Dec;28(4):435-42
pubmed: 19577632
Reprod Toxicol. 2011 May;31(4):409-17
pubmed: 21182934
Endocrinology. 2017 Jan 1;158(1):21-30
pubmed: 27841950
Reprod Toxicol. 2002 Mar-Apr;16(2):117-22
pubmed: 11955942
Endocrinology. 2008 Mar;149(3):1358-65
pubmed: 18039781
Toxicol Sci. 2014 Jul;140(1):190-203
pubmed: 24752507
Endocrinology. 2016 May;157(5):1736-9
pubmed: 27149041
PLoS One. 2012;7(5):e36129
pubmed: 22570695
Environ Res. 2016 Apr;146:245-51
pubmed: 26775005
Environ Res. 2021 Jan;192:110345
pubmed: 33096061
Nat Neurosci. 2013 Mar;16(3):281-9
pubmed: 23354331
Pediatrics. 2009 May;123(5):e932-9
pubmed: 19403485
Birth Defects Res B Dev Reprod Toxicol. 2012 Apr;95(2):123-9
pubmed: 22140080
Reprod Toxicol. 2016 Jun;61:186-94
pubmed: 27049580
Reprod Toxicol. 2010 Sep;30(2):313-21
pubmed: 20420898
Biol Reprod. 2018 Jan 1;98(1):130-145
pubmed: 29165555
Bioinformatics. 2011 Jun 1;27(11):1571-2
pubmed: 21493656
J Steroid Biochem Mol Biol. 2016 Apr;158:220-230
pubmed: 26658420
Environ Health Perspect. 2009 Dec;117(12):1839-46
pubmed: 20049201
Environ Toxicol Pharmacol. 2009 May;27(3):410-4
pubmed: 21783972
Endocr Rev. 2003 Oct;24(5):668-93
pubmed: 14570750
Sci Total Environ. 2020 Apr 10;712:134406
pubmed: 31927438
Front Endocrinol (Lausanne). 2018 Apr 06;9:148
pubmed: 29681889
Environ Int. 2021 Jan;146:106172
pubmed: 33113465
Endocrinology. 1984 May;114(5):1941-3
pubmed: 6370671
Arch Toxicol. 2018 Jan;92(1):501-512
pubmed: 28871463
PLoS One. 2012;7(9):e46249
pubmed: 23049995
Environ Health Perspect. 2021 Jan;129(1):17008
pubmed: 33502250
Endocrinology. 2018 Feb 1;159(2):795-809
pubmed: 29228129
Neurotoxicology. 2012 Jan;33(1):23-36
pubmed: 22101008
Reprod Toxicol. 2004 Aug-Sep;18(6):803-11
pubmed: 15279878
Endocrinology. 2016 May;157(5):1740-50
pubmed: 26950200
Endocrinology. 2013 Nov;154(11):4340-51
pubmed: 24002038
Environ Health Perspect. 2013 Jun;121(6):663-9
pubmed: 23512349
Ecotoxicol Environ Saf. 2019 Oct 15;181:362-369
pubmed: 31212184
PLoS One. 2008 May 21;3(5):e2210
pubmed: 18493313
J Endocrinol. 2014 Feb 10;220(3):375-88
pubmed: 24403293
Environ Health Perspect. 2011 Apr;119(4):547-52
pubmed: 21126938
Neuron. 2018 Apr 4;98(1):192-207.e10
pubmed: 29621487
Theriogenology. 2020 Jan 15;142:138-148
pubmed: 31593881

Auteurs

David López-Rodríguez (D)

GIGA Neurosciences, Neuroendocrinology Unit, University of Liège, Liège, Belgium.

Carlos Francisco Aylwin (CF)

Division of Neuroscience, Oregon National Primate Research Center, Oregon Health & Science University (OHSU), Portland, Oregon, USA.

Elena Sevrin (E)

GIGA Neurosciences, Neuroendocrinology Unit, University of Liège, Liège, Belgium.

Marzia Campanile (M)

GIGA Neurosciences, Neuroendocrinology Unit, University of Liège, Liège, Belgium.

Marion Martin (M)

Lille Neuroscience & Cognition (LilNCog), Institut national de la santé et de la recherche médicale (Inserm), CHU Lille, Lille, France.

Delphine Franssen (D)

GIGA Neurosciences, Neuroendocrinology Unit, University of Liège, Liège, Belgium.

Arlette Gérard (A)

GIGA Neurosciences, Neuroendocrinology Unit, University of Liège, Liège, Belgium.

Silvia Blacher (S)

Tumor and Development Biology, GIGA-Cancer, University of Liège, Liège, Belgium.

Ezio Tirelli (E)

Department of Psychology: Cognition and Behavior, University of Liège, Liège, Belgium.

Agnès Noël (A)

Tumor and Development Biology, GIGA-Cancer, University of Liège, Liège, Belgium.

Alejandro Lomniczi (A)

Division of Neuroscience, Oregon National Primate Research Center, Oregon Health & Science University (OHSU), Portland, Oregon, USA.

Anne-Simone Parent (AS)

GIGA Neurosciences, Neuroendocrinology Unit, University of Liège, Liège, Belgium.
Department of Pediatrics, University Hospital Liège, Liège, Belgium.

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Classifications MeSH