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RNA-induced inflammation and migration of precursor neurons initiates neuronal circuit regeneration in zebrafish

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  • Celia Vandestadt, Monash University
  • ,
  • Gilles C. Vanwalleghem
  • Mitra Amiri Khabooshan, Monash University
  • ,
  • Alon M. Douek, Monash University
  • ,
  • Hozana Andrade Castillo, Monash University, Centro Nacional de Pesquisa em Energia e Materiais
  • ,
  • Mei Li, Monash University
  • ,
  • Keith Schulze, Monash University
  • ,
  • Emily Don, Macquarie University
  • ,
  • Sebastian Alexander Stamatis, Monash University
  • ,
  • Madara Ratnadiwakara, Hudson Institute of Medical Research
  • ,
  • Minna Liisa Änkö, Hudson Institute of Medical Research, Monash University
  • ,
  • Ethan K. Scott, University of Queensland
  • ,
  • Jan Kaslin, Monash University

Tissue regeneration and functional restoration after injury are considered as stem- and progenitor-cell-driven processes. In the central nervous system, stem cell-driven repair is slow and problematic because function needs to be restored rapidly for vital tasks. In highly regenerative vertebrates, such as zebrafish, functional recovery is rapid, suggesting a capability for fast cell production and functional integration. Surprisingly, we found that migration of dormant “precursor neurons” to the injury site pioneers functional circuit regeneration after spinal cord injury and controls the subsequent stem-cell-driven repair response. Thus, the precursor neurons make do before the stem cells make new. Furthermore, RNA released from the dying or damaged cells at the site of injury acts as a signal to attract precursor neurons for repair. Taken together, our data demonstrate an unanticipated role of neuronal migration and RNA as drivers of neural repair.

Original languageEnglish
JournalDevelopmental Cell
Volume56
Issue16
Pages (from-to)2364-2380.e8
ISSN1534-5807
DOIs
Publication statusPublished - Aug 2021
Externally publishedYes

Bibliographical note

Funding Information:
Authors thank Monash Micro Imaging Facility and AquaCore aquatic animal facility ( Monash University ) for excellent technical support and Dr. Oliver Thorn-Seshold (Ludwig Maximilian Universität München) for generously donating the photostatin. The Australian Regenerative Medicine Institute is supported by grants from the State Government of Victoria and the Australian Government. J.K. was funded by NHMRC project grants GNT1068411 , GNT1145048 , and GNT 1138870 , Australia. E.K.S. was supported by NHMRC project grant APP1165173 , ARC Discovery Project grants DP140102036 and DP110103612 , and the Australian National Fabrication Facility , QLD node. H.A.C. was supported by fellowships from CNPq ( 202130/2015-0 ) and São Paulo Research Foundation (FAPESP – 2017/06022-7 ), Brasil.

Funding Information:
Authors thank Monash Micro Imaging Facility and AquaCore aquatic animal facility (Monash University) for excellent technical support and Dr. Oliver Thorn-Seshold (Ludwig Maximilian Universit?t M?nchen) for generously donating the photostatin. The Australian Regenerative Medicine Institute is supported by grants from the State Government of Victoria and the Australian Government. J.K. was funded by NHMRC project grants GNT1068411, GNT1145048, and GNT 1138870, Australia. E.K.S. was supported by NHMRC project grant APP1165173, ARC Discovery Project grants DP140102036 and DP110103612, and the Australian National Fabrication Facility, QLD node. H.A.C. was supported by fellowships from CNPq (202130/2015-0) and S?o Paulo Research Foundation (FAPESP ? 2017/06022-7), Brasil. Conceptualization, C.V. and J.K.; methodology, C.V. J.K. A.M.D. E.D. M.A.K. H.A.C. G.C.V. M.L. and M.-L.A.; software, C.V. K.S. G.C.V. E.K.S. and J.K.; validation, C.V. H.A.C. M.A.K. G.C.V. S.S. A.M.D. and J.K.; formal analysis, C.V. G.C.V. M.L. M.A.K. J.K. M.-L.A. and H.C.; investigation, C.V. M.A.K. H.A.C. G.C.V. A.M.D. M.L. S.S. M.R. E.D. J.K. and M.-L.A.; resources, J.K. E.K.S. and M.A.; data curation, C.V. G.C.V. and J.K.; writing ? original draft, J.K. and C.V.; writing ? review & editing, C.V. J.K. M.-L.A. A.M.D. H.A.C. and M.A.K.; visualization, C.V. G.C.V. J.K. M.A.K. and H.A.C.; supervision, J.K. M.-L.A. and E.K.S.; project administration, C.V. and J.K.; funding acquisition, J.K. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in science. One or more of the authors of this paper self-identifies as a member of the LGBTQ+ community.

Publisher Copyright:
© 2021 Elsevier Inc.

    Research areas

  • adult neurogenesis, dsRNA, epimorphic, innate immunity, morphallactic, neural stem cell, repair, spinal cord, SRC, TLR3

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