Material transfer is an essential form of intercellular communication to exchange information and resources between cells. Material transfer between neurons and from glia to neurons has been demonstrated to support neuronal survival and activity. Understanding the extent of material transfer in the healthy nervous system is limited. Here we report that in the mouse central nervous system (CNS), neurons receive nuclear and ribosomal material of Sox10-lineage cell (SOL) origin. We show that transfer of SOL-derived material to neurons is region dependent, establishes during postnatal brain maturation, and dynamically responds to LPS-induced neuroinflammation in the adult mouse brain. We identified satellite oligodendrocyte–neuron pairs with loss of plasma membrane integrity between nuclei, suggesting direct material transfer. Together, our findings provide evidence of regionally coordinated transfer of SOL-derived nuclear and ribosomal material to neurons in the mouse CNS, with potential implications for the understanding and modulation of neuronal function and treatment of neurological disorders.
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3 July 2023
Brief Definitive Report|
April 17 2023
Transfer of nuclear and ribosomal material from Sox10-lineage cells to neurons in the mouse brain
In Special Collection:
Neuroimmunology and Neurodegeneration 2023
Florian Mayrhofer
,
(Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing)
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
Florian Mayrhofer: fmayrhofer@gmail.com
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Angela M. Hanson
,
Angela M. Hanson
(Investigation)
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
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Manuel F. Navedo
,
Manuel F. Navedo
(Investigation, Writing - review & editing)
3Department of Pharmacology,
University of California, Davis
, Davis, CA, USA
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Yang K. Xiang
,
Yang K. Xiang
(Data curation, Methodology)
3Department of Pharmacology,
University of California, Davis
, Davis, CA, USA
4
Northern California Health Care System
, Mather, CA, USA
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Athena M. Soulika
,
Athena M. Soulika
(Data curation, Formal analysis, Methodology, Resources)
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
5Department of Dermatology,
University of California, Davis
, Sacramento, CA, USA
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Wenbin Deng
,
Wenbin Deng
(Funding acquisition, Project administration, Resources, Supervision, Writing - review & editing)
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
2Department of Biochemistry and Molecular Medicine,
School of Medicine, University of California, Davis
, Sacramento, CA, USA
6
School of Pharmaceutical Sciences, Shenzhen Campus of Sun Yat-sen University
, Guangdong, China
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Olga V. Chechneva
(Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing)
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
2Department of Biochemistry and Molecular Medicine,
School of Medicine, University of California, Davis
, Sacramento, CA, USA
Correspondence to Olga V. Chechneva: chechneva@gmail.com
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Florian Mayrhofer
Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
Angela M. Hanson
Investigation
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
Manuel F. Navedo
Investigation, Writing - review & editing
3Department of Pharmacology,
University of California, Davis
, Davis, CA, USA
Yang K. Xiang
Data curation, Methodology
3Department of Pharmacology,
University of California, Davis
, Davis, CA, USA
4
Northern California Health Care System
, Mather, CA, USA
Athena M. Soulika
Data curation, Formal analysis, Methodology, Resources
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
5Department of Dermatology,
University of California, Davis
, Sacramento, CA, USA
Wenbin Deng
Funding acquisition, Project administration, Resources, Supervision, Writing - review & editing
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
2Department of Biochemistry and Molecular Medicine,
School of Medicine, University of California, Davis
, Sacramento, CA, USA
6
School of Pharmaceutical Sciences, Shenzhen Campus of Sun Yat-sen University
, Guangdong, China
Olga V. Chechneva
Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing
1
Institute for Pediatric Regenerative Medicine, Shriners Children’s Northern California
, Sacramento, CA, USA
2Department of Biochemistry and Molecular Medicine,
School of Medicine, University of California, Davis
, Sacramento, CA, USA
Correspondence to Olga V. Chechneva: chechneva@gmail.com
Florian Mayrhofer: fmayrhofer@gmail.com
Disclosures: The authors declare no competing interests exist.
Received:
September 20 2022
Revision Received:
February 22 2023
Accepted:
March 27 2023
Online ISSN: 1540-9538
Print ISSN: 0022-1007
Funding
Funder(s):
Shriners Hospitals for Children
- Award Id(s): NC-87310,85114-NCA
Funder(s):
National Institutes of Health
- Award Id(s): R01HL149127,R01GM129376,R01HD087566,R01HD091325
Funder(s):
National Multiple Sclerosis Society
- Award Id(s): RG-1701-26770
© 2023 Mayrhofer et al.
2023
Mayrhofer et al.
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Exp Med (2023) 220 (7): e20221632.
Article history
Received:
September 20 2022
Revision Received:
February 22 2023
Accepted:
March 27 2023
Connected Content
Citation
Florian Mayrhofer, Angela M. Hanson, Manuel F. Navedo, Yang K. Xiang, Athena M. Soulika, Wenbin Deng, Olga V. Chechneva; Transfer of nuclear and ribosomal material from Sox10-lineage cells to neurons in the mouse brain. J Exp Med 3 July 2023; 220 (7): e20221632. doi: https://doi.org/10.1084/jem.20221632
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