Neural precursor cells tune striatal connectivity through the release of IGFBPL1.


Journal

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

Informations de publication

Date de publication:
08 12 2022
Historique:
received: 23 07 2021
accepted: 30 11 2022
entrez: 9 12 2022
pubmed: 10 12 2022
medline: 15 12 2022
Statut: epublish

Résumé

The adult brain retains over life endogenous neural stem/precursor cells (eNPCs) within the subventricular zone (SVZ). Whether or not these cells exert physiological functions is still unclear. In the present work, we provide evidence that SVZ-eNPCs tune structural, electrophysiological, and behavioural aspects of striatal function via secretion of insulin-like growth factor binding protein-like 1 (IGFBPL1). In mice, selective ablation of SVZ-eNPCs or selective abrogation of IGFBPL1 determined an impairment of striatal medium spiny neuron morphology, a higher failure rate in GABAergic transmission mediated by fast-spiking interneurons, and striatum-related behavioural dysfunctions. We also found IGFBPL1 expression in the human SVZ, foetal and induced-pluripotent stem cell-derived NPCs. Finally, we found a significant correlation between SVZ damage, reduction of striatum volume, and impairment of information processing speed in neurological patients. Our results highlight the physiological role of adult SVZ-eNPCs in supporting cognitive functions by regulating striatal neuronal activity.

Identifiants

pubmed: 36482070
doi: 10.1038/s41467-022-35341-y
pii: 10.1038/s41467-022-35341-y
pmc: PMC9731988
doi:

Substances chimiques

IGFBPL1 protein, human 0
Insulin-Like Growth Factor Binding Proteins 0
Tumor Suppressor Proteins 0
IGFBPL-1 protein, mouse 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

7579

Informations de copyright

© 2022. The Author(s).

Références

Neuropathol Appl Neurobiol. 1999 Jun;25(3):215-25
pubmed: 10417663
Proc Natl Acad Sci U S A. 2008 Dec 30;105(52):20994-9
pubmed: 19095802
Brain Behav. 2014 Jan;4(1):29-40
pubmed: 24653952
Bioinformatics. 2021 Apr 20;37(3):422-423
pubmed: 32745185
Biol Psychiatry. 2019 Dec 1;86(11):836-847
pubmed: 31471038
Science. 2014 Oct 3;346(6205):89-93
pubmed: 25147279
Rocz Akad Med Bialymst. 1998;43:5-26
pubmed: 9972040
Seizure. 2015 Apr;27:30-9
pubmed: 25891924
Brain. 2015 May;138(Pt 5):1239-46
pubmed: 25823475
Behav Brain Res. 2013 Oct 15;255:44-54
pubmed: 23628212
Mol Cell Neurosci. 2010 Mar;43(3):268-80
pubmed: 19969087
Nat Neurosci. 2008 Oct;11(10):1153-61
pubmed: 18758458
Brain. 2011 Jun;134(Pt 6):1585-7
pubmed: 21616966
Neuroscience. 2017 Mar 6;344:346-359
pubmed: 28057534
Front Neurosci. 2014 Apr 23;8:85
pubmed: 24795559
Nat Neurosci. 2012 Jul 26;15(8):1078-87
pubmed: 22837038
Neuron. 2017 Mar 22;93(6):1451-1463.e4
pubmed: 28334608
Front Neuroanat. 2018 Nov 08;12:91
pubmed: 30467465
Neurol Sci. 2010 Nov;31(Suppl 2):S211-4
pubmed: 20640466
Nat Neurosci. 1999 May;2(5):467-72
pubmed: 10321252
Cell Rep. 2018 Aug 21;24(8):2179-2190.e7
pubmed: 30134177
Biochem Insights. 2019 Apr 17;12:1178626419842176
pubmed: 31024217
Nature. 2020 Aug;584(7820):244-251
pubmed: 32728217
Nat Rev Neurosci. 2001 Oct;2(10):704-16
pubmed: 11584308
Sci Rep. 2018 Feb 1;8(1):2054
pubmed: 29391597
Brain. 2007 Oct;130(Pt 10):2543-53
pubmed: 17626034
Ann Neurol. 1982 Jun;11(6):599-607
pubmed: 7114809
Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2020 Jul;27(4):581-594
pubmed: 31411534
Cell Rep. 2019 Jan 8;26(2):394-406.e5
pubmed: 30625322
CNS Drugs. 2018 Jun;32(6):543-558
pubmed: 29926371
Biophys J. 1994 Jan;66(1):259-67
pubmed: 8130344
Science. 2004 Jun 25;304(5679):1926-9
pubmed: 15218136
Nature. 2003 Apr 17;422(6933):688-94
pubmed: 12700753
Genome Biol. 2018 Feb 6;19(1):15
pubmed: 29409532
Lancet Neurol. 2018 Feb;17(2):162-173
pubmed: 29275977
Cell. 2016 Jul 28;166(3):703-715
pubmed: 27453468
J Neurosci. 2016 Feb 03;36(5):1647-59
pubmed: 26843646
Mult Scler. 2017 Apr;23(5):721-733
pubmed: 28206827
Nat Commun. 2017 Oct 31;8(1):1229
pubmed: 29089485
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
J Neurosci. 2005 Nov 23;25(47):10884-93
pubmed: 16306401
Neuron. 2016 Oct 5;92(1):84-92
pubmed: 27710792
Nat Rev Neurosci. 2006 May;7(5):395-406
pubmed: 16760919
Nat Methods. 2019 Dec;16(12):1289-1296
pubmed: 31740819
J Neurosci. 2019 Jul 10;39(28):5481-5492
pubmed: 31138656
Stem Cells Dev. 2012 Jul 20;21(11):1831-7
pubmed: 22122665
J Neurosci. 2008 May 21;28(21):5504-12
pubmed: 18495884
Neuroimage. 2017 May 15;152:450-466
pubmed: 28284799
Neuron. 2010 Aug 12;67(3):466-79
pubmed: 20696383
J Clin Invest. 2014 Mar;124(3):1228-41
pubmed: 24569378
Brain. 2012 Nov;135(Pt 11):3320-35
pubmed: 23008234
Mult Scler Relat Disord. 2019 Jun;31:93-96
pubmed: 30953954
Mov Disord. 1996 Mar;11(2):136-42
pubmed: 8684382
Nat Rev Neurosci. 2019 Aug;20(8):482-494
pubmed: 31171839
J Neurosci. 2005 May 11;25(19):4801-5
pubmed: 15888655
Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11050-5
pubmed: 10984517
Nat Neurosci. 2005 Sep;8(9):1179-87
pubmed: 16116450
Nat Neurosci. 2012 Nov;15(11):1485-7
pubmed: 23086334
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
pubmed: 16199517
Harv Rev Psychiatry. 2017 Nov/Dec;25(6):270-278
pubmed: 29117022
Cell Syst. 2019 Apr 24;8(4):281-291.e9
pubmed: 30954476
Ann Neurol. 2019 Mar;85(3):340-351
pubmed: 30719730
J Neurol Sci. 2006 Jun 15;245(1-2):41-6
pubmed: 16643953
Cell. 2013 Jun 6;153(6):1219-1227
pubmed: 23746839
J Neurosci. 2009 Apr 15;29(15):5032-43
pubmed: 19369572
Genome Res. 2012 Sep;22(9):1760-74
pubmed: 22955987
Nat Rev Neurosci. 2001 Apr;2(4):229-39
pubmed: 11283746
Nat Cell Biol. 2011 Jul 31;13(9):1076-83
pubmed: 21804544
Mult Scler. 2006 Dec;12(6):787-93
pubmed: 17263008
Nat Rev Neurosci. 2010 May;11(5):316-28
pubmed: 20404840
Neurosci Lett. 2010 Jan 22;469(2):214-8
pubmed: 19962428
Genome Res. 2017 Mar;27(3):491-499
pubmed: 28100584
Neuroimage. 2017 Jul 15;155:159-168
pubmed: 28435096
Brain Res. 1997 Sep 19;769(1):97-107
pubmed: 9374277
Brain Res. 2020 Mar 1;1730:146619
pubmed: 31874148
Cell. 1999 Jun 11;97(6):703-16
pubmed: 10380923
J Clin Invest. 2014 Mar;124(3):970-3
pubmed: 24569367
Circ Res. 2019 Feb 15;124(4):511-525
pubmed: 30591003
J Int Neuropsychol Soc. 2015 Mar;21(3):193-202
pubmed: 25850430
Brain. 2008 Oct;131(Pt 10):2564-78
pubmed: 18757884
EMBO J. 2019 Mar 15;38(6):
pubmed: 30643018
PLoS Biol. 2015 Jan 26;13(1):e1002045
pubmed: 25621867
J Anat. 1953 Oct;87(4):387-406
pubmed: 13117757
Cell Stem Cell. 2008 Sep 11;3(3):279-88
pubmed: 18786415
Front Neurosci. 2016 Feb 23;10:52
pubmed: 26941597
Trends Neurosci. 2003 Aug;26(8):436-43
pubmed: 12900175
Neuron. 1999 Jun;23(2):399-409
pubmed: 10399944
Nature. 2004 Feb 19;427(6976):740-4
pubmed: 14973487
Science. 2019 Nov 29;366(6469):1134-1139
pubmed: 31727856
Neuron. 2016 Jul 20;91(2):260-92
pubmed: 27477017
Cell. 2017 Nov 16;171(5):1191-1205.e28
pubmed: 29149606
Nat Biotechnol. 2022 Feb;40(2):235-244
pubmed: 34635836

Auteurs

Erica Butti (E)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.

Stefano Cattaneo (S)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.
Vita-Salute San Raffaele University, Milan, Italy.

Marco Bacigaluppi (M)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.
Vita-Salute San Raffaele University, Milan, Italy.

Marco Cambiaghi (M)

Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy.

Giulia Maria Scotti (GM)

Omics Sciences Center, IRCCS San Raffaele Hospital, Milan, Italy.

Elena Brambilla (E)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.

Francesca Ruffini (F)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.

Giacomo Sferruzza (G)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.

Maddalena Ripamonti (M)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.
Vita-Salute San Raffaele University, Milan, Italy.

Fabio Simeoni (F)

Omics Sciences Center, IRCCS San Raffaele Hospital, Milan, Italy.

Laura Cacciaguerra (L)

Neuroimaging Research Unit, Institute of Experimental Neurology (INSPE), Division of Neuroscience, IRCCS San Raffaele Hospital, Milan, Italy.

Aurora Zanghì (A)

Neuroimaging Research Unit, Institute of Experimental Neurology (INSPE), Division of Neuroscience, IRCCS San Raffaele Hospital, Milan, Italy.

Angelo Quattrini (A)

Neuropathology Unit, Institute of Experimental Neurology (INSPE), Division of Neuroscience, IRCCS San Raffaele Hospital, Milan, Italy.

Riccardo Fesce (R)

Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy.

Paola Panina-Bordignon (P)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.
Vita-Salute San Raffaele University, Milan, Italy.

Francesca Giannese (F)

Omics Sciences Center, IRCCS San Raffaele Hospital, Milan, Italy.

Davide Cittaro (D)

Omics Sciences Center, IRCCS San Raffaele Hospital, Milan, Italy.

Tanja Kuhlmann (T)

Institute of Neuropathology, University Hospital Muster, Muster, Germany.

Patrizia D'Adamo (P)

Molecular genetics of Intellectual Disability, Division of Neuroscience, IRCCS San Raffaele Hospital, Milan, Italy.

Maria Assunta Rocca (MA)

Vita-Salute San Raffaele University, Milan, Italy.
Neuroimaging Research Unit, Institute of Experimental Neurology (INSPE), Division of Neuroscience, IRCCS San Raffaele Hospital, Milan, Italy.

Stefano Taverna (S)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy.

Gianvito Martino (G)

Neuroimmunology Unit, Division of Neuroscience, Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital, Milan, Italy. martino.gianvito@hsr.it.
Vita-Salute San Raffaele University, Milan, Italy. martino.gianvito@hsr.it.

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