IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35341-y.html
   My bibliography  Save this article

Neural precursor cells tune striatal connectivity through the release of IGFBPL1

Author

Listed:
  • Erica Butti

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital)

  • Stefano Cattaneo

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital
    Vita-Salute San Raffaele University)

  • Marco Bacigaluppi

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital
    Vita-Salute San Raffaele University)

  • Marco Cambiaghi

    (University of Verona)

  • Giulia Maria Scotti

    (IRCCS San Raffaele Hospital)

  • Elena Brambilla

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital)

  • Francesca Ruffini

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital)

  • Giacomo Sferruzza

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital)

  • Maddalena Ripamonti

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital
    Vita-Salute San Raffaele University)

  • Fabio Simeoni

    (IRCCS San Raffaele Hospital)

  • Laura Cacciaguerra

    (Institute of Experimental Neurology (INSPE), Division of Neuroscience, IRCCS San Raffaele Hospital)

  • Aurora Zanghì

    (Institute of Experimental Neurology (INSPE), Division of Neuroscience, IRCCS San Raffaele Hospital)

  • Angelo Quattrini

    (Division of Neuroscience, IRCCS San Raffaele Hospital)

  • Riccardo Fesce

    (Humanitas University, Pieve Emanuele)

  • Paola Panina-Bordignon

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital
    Vita-Salute San Raffaele University)

  • Francesca Giannese

    (IRCCS San Raffaele Hospital)

  • Davide Cittaro

    (IRCCS San Raffaele Hospital)

  • Tanja Kuhlmann

    (University Hospital Muster)

  • Patrizia D’Adamo

    (Division of Neuroscience, IRCCS San Raffaele Hospital)

  • Maria Assunta Rocca

    (Vita-Salute San Raffaele University
    Institute of Experimental Neurology (INSPE), Division of Neuroscience, IRCCS San Raffaele Hospital)

  • Stefano Taverna

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital)

  • Gianvito Martino

    (Institute of Experimental Neurology (INSPE), IRCCS San Raffaele Hospital
    Vita-Salute San Raffaele University)

Abstract

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.

Suggested Citation

  • Erica Butti & Stefano Cattaneo & Marco Bacigaluppi & Marco Cambiaghi & Giulia Maria Scotti & Elena Brambilla & Francesca Ruffini & Giacomo Sferruzza & Maddalena Ripamonti & Fabio Simeoni & Laura Cacci, 2022. "Neural precursor cells tune striatal connectivity through the release of IGFBPL1," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35341-y
    DOI: 10.1038/s41467-022-35341-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35341-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-35341-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Wouter Meuleman & Alexander Muratov & Eric Rynes & Jessica Halow & Kristen Lee & Daniel Bates & Morgan Diegel & Douglas Dunn & Fidencio Neri & Athanasios Teodosiadis & Alex Reynolds & Eric Haugen & Je, 2020. "Index and biological spectrum of human DNase I hypersensitive sites," Nature, Nature, vol. 584(7820), pages 244-251, August.
    2. Mattia Ferro & Jacopo Lamanna & Maddalena Ripamonti & Gabriella Racchetti & Alessandro Arena & Sara Spadini & Giovanni Montesano & Riccardo Cortese & Vincenzo Zimarino & Antonio Malgaroli, 2017. "Functional mapping of brain synapses by the enriching activity-marker SynaptoZip," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    3. Stefano Pluchino & Angelo Quattrini & Elena Brambilla & Angela Gritti & Giuliana Salani & Giorgia Dina & Rossella Galli & Ubaldo Del Carro & Stefano Amadio & Alessandra Bergami & Roberto Furlan & Gian, 2003. "Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis," Nature, Nature, vol. 422(6933), pages 688-694, April.
    4. Nader Sanai & Anthony D. Tramontin & Alfredo Quiñones-Hinojosa & Nicholas M. Barbaro & Nalin Gupta & Sandeep Kunwar & Michael T. Lawton & Michael W. McDermott & Andrew T. Parsa & José Manuel-García Ve, 2004. "Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration," Nature, Nature, vol. 427(6976), pages 740-744, February.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Michael R. Williamson & Stephanie P. Le & Ronald L. Franzen & Nicole A. Donlan & Jill L. Rosow & Mathilda S. Nicot-Cartsonis & Alexis Cervantes & Benjamin Deneen & Andrew K. Dunn & Theresa A. Jones & , 2023. "Subventricular zone cytogenesis provides trophic support for neural repair in a mouse model of stroke," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Denis Houzelstein & Caroline Eozenou & Carlos F. Lagos & Maëva Elzaiat & Joelle Bignon-Topalovic & Inma Gonzalez & Vincent Laville & Laurène Schlick & Somboon Wankanit & Prochi Madon & Jyotsna Kirtane, 2024. "A conserved NR5A1-responsive enhancer regulates SRY in testis-determination," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Chirag Nepal & Jesper B. Andersen, 2023. "Alternative promoters in CpG depleted regions are prevalently associated with epigenetic misregulation of liver cancer transcriptomes," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Milton Pividori & Sumei Lu & Binglan Li & Chun Su & Matthew E. Johnson & Wei-Qi Wei & Qiping Feng & Bahram Namjou & Krzysztof Kiryluk & Iftikhar J. Kullo & Yuan Luo & Blair D. Sullivan & Benjamin F. V, 2023. "Projecting genetic associations through gene expression patterns highlights disease etiology and drug mechanisms," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Hillary Koch & Cheryl A. Keller & Guanjue Xiang & Belinda Giardine & Feipeng Zhang & Yicheng Wang & Ross C. Hardison & Qunhua Li, 2022. "CLIMB: High-dimensional association detection in large scale genomic data," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Warren A. Cheung & Adam F. Johnson & William J. Rowell & Emily Farrow & Richard Hall & Ana S. A. Cohen & John C. Means & Tricia N. Zion & Daniel M. Portik & Christopher T. Saunders & Boryana Koseva & , 2023. "Direct haplotype-resolved 5-base HiFi sequencing for genome-wide profiling of hypermethylation outliers in a rare disease cohort," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Ingrid M. Saldana-Guerrero & Luis F. Montano-Gutierrez & Katy Boswell & Christoph Hafemeister & Evon Poon & Lisa E. Shaw & Dylan Stavish & Rebecca A. Lea & Sara Wernig-Zorc & Eva Bozsaky & Irfete S. F, 2024. "A human neural crest model reveals the developmental impact of neuroblastoma-associated chromosomal aberrations," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    8. Lucia Trastulla & Georgii Dolgalev & Sylvain Moser & Laura T. Jiménez-Barrón & Till F. M. Andlauer & Moritz Scheidt & Monika Budde & Urs Heilbronner & Sergi Papiol & Alexander Teumer & Georg Homuth & , 2024. "Distinct genetic liability profiles define clinically relevant patient strata across common diseases," Nature Communications, Nature, vol. 15(1), pages 1-28, December.
    9. Derek Wong & Maha Tageldein & Ping Luo & Erik Ensminger & Jeffrey Bruce & Leslie Oldfield & Haifan Gong & Nicholas William Fischer & Brianne Laverty & Vallijah Subasri & Scott Davidson & Reem Khan & A, 2024. "Cell-free DNA from germline TP53 mutation carriers reflect cancer-like fragmentation patterns," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Samir Rachid Zaim & Mark-Phillip Pebworth & Imran McGrath & Lauren Okada & Morgan Weiss & Julian Reading & Julie L. Czartoski & Troy R. Torgerson & M. Juliana McElrath & Thomas F. Bumol & Peter J. Ske, 2024. "MOCHA’s advanced statistical modeling of scATAC-seq data enables functional genomic inference in large human cohorts," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    11. Anna-Lisa Doebley & Minjeong Ko & Hanna Liao & A. Eden Cruikshank & Katheryn Santos & Caroline Kikawa & Joseph B. Hiatt & Robert D. Patton & Navonil De Sarkar & Katharine A. Collier & Anna C. H. Hoge , 2022. "A framework for clinical cancer subtyping from nucleosome profiling of cell-free DNA," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    12. Kaela M. Varberg & Esteban M. Dominguez & Boryana Koseva & Joseph M. Varberg & Ross P. McNally & Ayelen Moreno-Irusta & Emily R. Wesley & Khursheed Iqbal & Warren A. Cheung & Carl Schwendinger-Schreck, 2023. "Extravillous trophoblast cell lineage development is associated with active remodeling of the chromatin landscape," Nature Communications, Nature, vol. 14(1), pages 1-23, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35341-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.