Pregnancy-induced maternal microchimerism shapes neurodevelopment and behavior in mice.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
05 08 2022
Historique:
received: 22 10 2021
accepted: 21 07 2022
entrez: 5 8 2022
pubmed: 6 8 2022
medline: 10 8 2022
Statut: epublish

Résumé

Life-long brain function and mental health are critically determined by developmental processes occurring before birth. During mammalian pregnancy, maternal cells are transferred to the fetus. They are referred to as maternal microchimeric cells (MMc). Among other organs, MMc seed into the fetal brain, where their function is unknown. Here, we show that, in the offspring's developing brain in mice, MMc express a unique signature of sensome markers, control microglia homeostasis and prevent excessive presynaptic elimination. Further, MMc facilitate the oscillatory entrainment of developing prefrontal-hippocampal circuits and support the maturation of behavioral abilities. Our findings highlight that MMc are not a mere placental leak out, but rather a functional mechanism that shapes optimal conditions for healthy brain function later in life.

Identifiants

pubmed: 35931682
doi: 10.1038/s41467-022-32230-2
pii: 10.1038/s41467-022-32230-2
pmc: PMC9356013
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4571

Informations de copyright

© 2022. The Author(s).

Références

Biol Reprod. 2008 May;78(5):883-7
pubmed: 18256332
Cereb Cortex. 2016 Oct 17;26(11):4265-4281
pubmed: 27613435
J Neurosci. 2013 Aug 28;33(35):14211-24
pubmed: 23986255
Science. 2020 Jul 31;369(6503):530-537
pubmed: 32732419
Blood. 2009 Oct 22;114(17):3578-87
pubmed: 19700665
Neuropsychopharmacology. 2019 Apr;44(5):859-868
pubmed: 30610191
Front Immunol. 2018 Mar 22;9:505
pubmed: 29623077
J Intellect Disabil Res. 2010 Mar;54(3):216-23
pubmed: 20136681
Genome Biol. 2015 Dec 10;16:278
pubmed: 26653891
J Vis Exp. 2013 Dec 24;(82):50978
pubmed: 24429507
Neuron. 2012 May 24;74(4):691-705
pubmed: 22632727
Neuron. 2020 Jan 8;105(1):60-74.e7
pubmed: 31733940
Neuron. 2021 Apr 21;109(8):1350-1364.e6
pubmed: 33675685
J Neurosci. 2019 Feb 13;39(7):1222-1235
pubmed: 30617212
Neuron. 2011 Jul 28;71(2):332-47
pubmed: 21791291
Chimerism. 2014;5(3-4):99-102
pubmed: 25483743
Behav Sci (Basel). 2018 Jan 18;8(1):
pubmed: 29346276
J Clin Invest. 2011 Feb;121(2):582-92
pubmed: 21245575
Anim Behav. 1965 Apr-Jul;13(2):234-41
pubmed: 5835840
Science. 2011 Sep 9;333(6048):1456-8
pubmed: 21778362
Cell. 2020 Mar 5;180(5):833-846.e16
pubmed: 32142677
Am J Obstet Gynecol. 2008 Mar;198(3):325.e1-6
pubmed: 18191801
Sci Rep. 2018 Sep 24;8(1):14289
pubmed: 30250150
Hypertension. 2020 Mar;75(3):748-754
pubmed: 31884857
Neuropsychopharmacology. 2015 Jun;40(7):1674-81
pubmed: 25578799
Nat Protoc. 2019 Dec;14(12):3506-3537
pubmed: 31748753
Neuron. 2018 Oct 10;100(1):120-134.e6
pubmed: 30308165
J Neurosci Res. 1999 May 15;56(4):441-6
pubmed: 10340751
Curr Protoc Microbiol. 2005 Oct;Appendix 3:Appendix 3C
pubmed: 18770544
Immunity. 2019 Jan 15;50(1):253-271.e6
pubmed: 30471926
Immunity. 2018 May 15;48(5):979-991.e8
pubmed: 29752066
J Clin Invest. 1999 Jul;104(1):41-7
pubmed: 10393697
Nature. 2014 May 22;509(7501):507-11
pubmed: 24828040
Dev Psychobiol. 2013 May;55(4):373-81
pubmed: 22553126
Genome Biol. 2014;15(12):550
pubmed: 25516281
Chimerism. 2014;5(3-4):68-74
pubmed: 25779065
Behav Brain Res. 2007 Feb 27;177(2):254-60
pubmed: 17204340
Behav Neural Biol. 1982 Jun;35(2):205-10
pubmed: 7150186
Am J Physiol Endocrinol Metab. 2004 Nov;287(5):E863-70
pubmed: 15238353
J Neurosci. 2016 Mar 23;36(12):3579-87
pubmed: 27013686
Nat Neurosci. 2013 Dec;16(12):1896-905
pubmed: 24162652
Lab Invest. 2003 May;83(5):673-81
pubmed: 12746477
Lancet. 2003 Nov 15;362(9396):1617-23
pubmed: 14630442
Semin Immunopathol. 2020 Aug;42(4):413-429
pubmed: 32894326
J Immunol Methods. 2014 Apr;406:74-82
pubmed: 24657636
J Immunol. 2009 Aug 1;183(3):1751-8
pubmed: 19587007
PLoS Biol. 2020 Aug 31;18(8):e3000820
pubmed: 32866173
Nature. 2015 Jun 18;522(7556):309-14
pubmed: 26053122
Nat Protoc. 2006;1(3):1117-9
pubmed: 17406392
Nat Commun. 2018 Jan 8;9(1):75
pubmed: 29311541
Nat Rev Neurosci. 2015 Jun;16(6):332-44
pubmed: 25921815
Chimerism. 2012 Jul-Dec;3(3):1-3
pubmed: 22992682
Nat Rev Immunol. 2017 Aug;17(8):483-494
pubmed: 28480895
Neurobiol Learn Mem. 2012 May;97(4):470-81
pubmed: 22521798
Nature. 2020 Oct;586(7828):281-286
pubmed: 32968276
Nat Commun. 2021 Aug 4;12(1):4706
pubmed: 34349112
J Pediatr. 2003 Jan;142(1):31-5
pubmed: 12520251
Nat Commun. 2017 Feb 20;8:14563
pubmed: 28216627
Proc Natl Acad Sci U S A. 2019 Oct 1;116(40):20190-20200
pubmed: 31527230
Nature. 2004 Jul 22;430(6998):419-21
pubmed: 15269759
Front Immunol. 2018 Sep 26;9:2186
pubmed: 30319639
Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):705-8
pubmed: 8570620
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
J Vis Exp. 2016 Nov 3;(117):
pubmed: 27842358
Trends Immunol. 2012 Aug;33(8):421-7
pubmed: 22609148
Neurosci Biobehav Rev. 2009 Apr;33(4):508-15
pubmed: 18771687
Nat Rev Neurosci. 2017 Sep;18(9):547-558
pubmed: 28655882
J Reprod Immunol. 2015 Apr;108:12-25
pubmed: 25638482
Placenta. 2012 Jan;33(1):39-46
pubmed: 22093381
Dev Psychobiol. 2013 Apr;55(3):294-308
pubmed: 22488119
Science. 2016 Aug 19;353(6301):aad8670
pubmed: 27338705
Cell. 2019 Jun 13;177(7):1888-1902.e21
pubmed: 31178118
Biol Psychiatry. 2007 Sep 1;62(5):446-54
pubmed: 17217927
Science. 2008 Dec 5;322(5907):1562-5
pubmed: 19056990
Nature. 2015 Feb 26;518(7540):547-51
pubmed: 25470051
Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1637-42
pubmed: 17244711
J Neuroinflammation. 2014 Sep 12;11:156
pubmed: 25212412
Mol Psychiatry. 2020 Oct;25(10):2330-2341
pubmed: 30610201

Auteurs

Steven Schepanski (S)

Division of Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Institute of Developmental Neurophysiology, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Mattia Chini (M)

Institute of Developmental Neurophysiology, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Veronika Sternemann (V)

Division of Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Institute of Developmental Neurophysiology, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Christopher Urbschat (C)

Division of Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Kristin Thiele (K)

Division of Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Ting Sun (T)

Institute of Medical Systems Biology, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Department of Neurogenetics, Max Planck Institute for Multidisciplinary Sciences, Göttingen, Germany.

Yu Zhao (Y)

Institute of Medical Systems Biology, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Mareike Poburski (M)

Division of Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Institute of Developmental Neurophysiology, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Anna Woestemeier (A)

Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Marie-Theres Thieme (MT)

Division of Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Dimitra E Zazara (DE)

Division of Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Malik Alawi (M)

Bioinformatics Service Facility, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Nicole Fischer (N)

Institute of Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Joerg Heeren (J)

Department of Biochemistry and Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Nikita Vladimirov (N)

Berlin Institute for Medical Systems Biology, Max Delbrück Center for Molecular Medicine, Berlin, Germany.

Andrew Woehler (A)

Berlin Institute for Medical Systems Biology, Max Delbrück Center for Molecular Medicine, Berlin, Germany.

Victor G Puelles (VG)

III Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Stefan Bonn (S)

Institute of Medical Systems Biology, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Nicola Gagliani (N)

Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Ileana L Hanganu-Opatz (IL)

Institute of Developmental Neurophysiology, Center for Molecular Neurobiology Hamburg (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany. hangop@zmnh.uni-hamburg.de.

Petra C Arck (PC)

Division of Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany. p.arck@uke.de.

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