ADF/Cofilin-Mediated Actin Turnover Promotes Axon Regeneration in the Adult CNS

Injured axons fail to regenerate in the adult CNS, which contrasts with their vigorous growth during embryonic development. We explored the potential of re-initiating axon extension after injury by reactivating the molecular mechanisms that drive morphogenetic transformation of neurons during develo...

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Published inNeuron (Cambridge, Mass.) Vol. 103; no. 6; pp. 1073 - 1085.e6
Main Authors Tedeschi, Andrea, Dupraz, Sebastian, Curcio, Michele, Laskowski, Claudia J., Schaffran, Barbara, Flynn, Kevin C., Santos, Telma E., Stern, Sina, Hilton, Brett J., Larson, Molly J.E., Gurniak, Christine B., Witke, Walter, Bradke, Frank
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 25.09.2019
Elsevier Limited
Subjects
Actin
actin dynamics
Actins - metabolism
ADF/cofilin
Animals
axon injury
axon regeneration
Axons
Axons - metabolism
Axons - pathology
Cofilin
Cofilin 1 - genetics
Cofilin 1 - metabolism
Cofilin 2 - genetics
Cofilin 2 - metabolism
conditioning
Destrin - genetics
Destrin - metabolism
Developmental plasticity
Embryogenesis
Genetic transformation
Growth Cones - metabolism
Growth Cones - pathology
Immunoglobulins
Intravital Microscopy
Mice
Microscopy
Microscopy, Confocal
Molecular modelling
Morphology
Nerve Regeneration - genetics
Neurons
Neurons - metabolism
Neurons - pathology
Rats
Regeneration
Spinal cord injuries
Spinal Cord Injuries - genetics
Spinal Cord Injuries - metabolism
Spinal Cord Injuries - pathology
Statistical analysis
Time-Lapse Imaging
Trauma
Variance analysis
axon regeneration
actin dynamics
ADF/cofilin
conditioning
axon injury
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Abstract Injured axons fail to regenerate in the adult CNS, which contrasts with their vigorous growth during embryonic development. We explored the potential of re-initiating axon extension after injury by reactivating the molecular mechanisms that drive morphogenetic transformation of neurons during development. Genetic loss- and gain-of-function experiments followed by time-lapse microscopy, in vivo imaging, and whole-mount analysis show that axon regeneration is fueled by elevated actin turnover. Actin depolymerizing factor (ADF)/cofilin controls actin turnover to sustain axon regeneration after spinal cord injury through its actin-severing activity. This pinpoints ADF/cofilin as a key regulator of axon growth competence, irrespective of developmental stage. These findings reveal the central role of actin dynamics regulation in this process and elucidate a core mechanism underlying axon growth after CNS trauma. Thereby, neurons maintain the capacity to stimulate developmental programs during adult life, expanding their potential for plasticity. Thus, actin turnover is a key process for future regenerative interventions. [Display omitted] •Elevated actin turnover is essential for regenerative growth•ADF/cofilin activity increases during conditioning-mediated regeneration•ADF/cofilin is necessary and sufficient for axon regeneration•The severing activity of ADF/cofilin is critical for axon regeneration Tedeschi et al. identify ADF/cofilin as a key driver of axon regeneration in adult dorsal root ganglion neurons. Specifically, enhanced actin turnover by the ADF/cofilin severing function controls axon regeneration in the adult CNS.
AbstractList Injured axons fail to regenerate in the adult CNS, which contrasts with their vigorous growth during embryonic development. We explored the potential of re-initiating axon extension after injury by reactivating the molecular mechanisms that drive morphogenetic transformation of neurons during development. Genetic loss- and gain-of-function experiments followed by time-lapse microscopy, in vivo imaging, and whole-mount analysis show that axon regeneration is fueled by elevated actin turnover. Actin depolymerizing factor (ADF)/cofilin controls actin turnover to sustain axon regeneration after spinal cord injury through its actin-severing activity. This pinpoints ADF/cofilin as a key regulator of axon growth competence, irrespective of developmental stage. These findings reveal the central role of actin dynamics regulation in this process and elucidate a core mechanism underlying axon growth after CNS trauma. Thereby, neurons maintain the capacity to stimulate developmental programs during adult life, expanding their potential for plasticity. Thus, actin turnover is a key process for future regenerative interventions. [Display omitted] •Elevated actin turnover is essential for regenerative growth•ADF/cofilin activity increases during conditioning-mediated regeneration•ADF/cofilin is necessary and sufficient for axon regeneration•The severing activity of ADF/cofilin is critical for axon regeneration Tedeschi et al. identify ADF/cofilin as a key driver of axon regeneration in adult dorsal root ganglion neurons. Specifically, enhanced actin turnover by the ADF/cofilin severing function controls axon regeneration in the adult CNS.
SummaryInjured axons fail to regenerate in the adult CNS, which contrasts with their vigorous growth during embryonic development. We explored the potential of re-initiating axon extension after injury by reactivating the molecular mechanisms that drive morphogenetic transformation of neurons during development. Genetic loss- and gain-of-function experiments followed by time-lapse microscopy, in vivo imaging, and whole-mount analysis show that axon regeneration is fueled by elevated actin turnover. Actin depolymerizing factor (ADF)/cofilin controls actin turnover to sustain axon regeneration after spinal cord injury through its actin-severing activity. This pinpoints ADF/cofilin as a key regulator of axon growth competence, irrespective of developmental stage. These findings reveal the central role of actin dynamics regulation in this process and elucidate a core mechanism underlying axon growth after CNS trauma. Thereby, neurons maintain the capacity to stimulate developmental programs during adult life, expanding their potential for plasticity. Thus, actin turnover is a key process for future regenerative interventions.
Injured axons fail to regenerate in the adult central nervous system, which contrasts their vigorous growth during embryonic development. We explored the potential of re-initiating axon extension after injury by reactivating the molecular mechanisms that drive morphogenetic transformation of neurons during development. Genetic loss- and gain-of-function experiments followed by time-lapse microscopy, in vivo imaging and whole-mount analysis show that axon regeneration is fueled by elevated actin turnover. ADF/Cofilin controls actin turnover to sustain axon regeneration after spinal cord injury through its actin-severing activity. This pinpoints ADF/Cofilin as a key regulator of axon growth competence, irrespective of developmental stage. These findings reveal the central role of actin dynamics regulation in this process and elucidate a core mechanism underlying axon growth after CNS trauma. Thereby, neurons maintain the capacity to stimulate developmental programs during adult life, expanding their potential for plasticity. Thus, actin turnover is a key process for future regenerative interventions. Tedeschi et al. identify ADF/Cofilin as a key driver of axon regeneration in adult dorsal root ganglion neurons. Specifically, enhanced actin turnover by the ADF/Cofilin severing function controls axon regeneration in the adult CNS.
Injured axons fail to regenerate in the adult CNS, which contrasts with their vigorous growth during embryonic development. We explored the potential of re-initiating axon extension after injury by reactivating the molecular mechanisms that drive morphogenetic transformation of neurons during development. Genetic loss- and gain-of-function experiments followed by time-lapse microscopy, in vivo imaging, and whole-mount analysis show that axon regeneration is fueled by elevated actin turnover. Actin depolymerizing factor (ADF)/cofilin controls actin turnover to sustain axon regeneration after spinal cord injury through its actin-severing activity. This pinpoints ADF/cofilin as a key regulator of axon growth competence, irrespective of developmental stage. These findings reveal the central role of actin dynamics regulation in this process and elucidate a core mechanism underlying axon growth after CNS trauma. Thereby, neurons maintain the capacity to stimulate developmental programs during adult life, expanding their potential for plasticity. Thus, actin turnover is a key process for future regenerative interventions.
Author Gurniak, Christine B.
Stern, Sina
Tedeschi, Andrea
Schaffran, Barbara
Curcio, Michele
Dupraz, Sebastian
Larson, Molly J.E.
Hilton, Brett J.
Bradke, Frank
Flynn, Kevin C.
Laskowski, Claudia J.
Santos, Telma E.
Witke, Walter
AuthorAffiliation 5 Present address: Stem Cells, R&D Systems, Inc. 614 McKinley Place NE, Minneapolis, MN 55413, USA
4 Present address: Klifovet AG, Geyerspergerstr. 27, 80689 Munich, Germany
1 Axonal Growth and Regeneration, German Center for Neurodegenerative Diseases (DZNE), Sigmund-Freud-Str. 27, 53127 Bonn, Germany
7 Lead Contact
3 Present address: VIB Discovery Sciences, Bio-Incubator Leuven, Gaston Geenslaan 1, 3001 Leuven (Heverlee), Belgium
2 Present address: Center for Brain and Spinal Cord Repair, Department of Neuroscience, Wexner Medical Center, The Ohio State University, 460 W 12th Ave, Columbus, OH 43210, USA
6 Institute of Genetics, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115 Bonn, Germany
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  organization: Axonal Growth and Regeneration, German Center for Neurodegenerative Diseases (DZNE), Sigmund-Freud-Str. 27, 53127 Bonn, Germany
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  givenname: Kevin C.
  surname: Flynn
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  organization: Axonal Growth and Regeneration, German Center for Neurodegenerative Diseases (DZNE), Sigmund-Freud-Str. 27, 53127 Bonn, Germany
– sequence: 7
  givenname: Telma E.
  surname: Santos
  fullname: Santos, Telma E.
  organization: Axonal Growth and Regeneration, German Center for Neurodegenerative Diseases (DZNE), Sigmund-Freud-Str. 27, 53127 Bonn, Germany
– sequence: 8
  givenname: Sina
  surname: Stern
  fullname: Stern, Sina
  organization: Axonal Growth and Regeneration, German Center for Neurodegenerative Diseases (DZNE), Sigmund-Freud-Str. 27, 53127 Bonn, Germany
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  givenname: Brett J.
  surname: Hilton
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  organization: Axonal Growth and Regeneration, German Center for Neurodegenerative Diseases (DZNE), Sigmund-Freud-Str. 27, 53127 Bonn, Germany
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  givenname: Molly J.E.
  surname: Larson
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  organization: Center for Brain and Spinal Cord Repair, Department of Neuroscience, Wexner Medical Center, The Ohio State University, 460 W. 12th Ave., Columbus, OH 43210, USA
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  givenname: Christine B.
  surname: Gurniak
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  organization: Institute of Genetics, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115 Bonn, Germany
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  surname: Witke
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  organization: Institute of Genetics, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115 Bonn, Germany
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  givenname: Frank
  surname: Bradke
  fullname: Bradke, Frank
  email: frank.bradke@dzne.de
  organization: Axonal Growth and Regeneration, German Center for Neurodegenerative Diseases (DZNE), Sigmund-Freud-Str. 27, 53127 Bonn, Germany
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31400829$$D View this record in MEDLINE/PubMed
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Issue 6
Keywords axon regeneration
actin dynamics
ADF/cofilin
conditioning
axon injury
Language English
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content type line 23
C.L., K.F., and F.B. conceived the project; A.T., S.D., M.C., C.L., B.S., and F.B. designed research; A.T., S.D., M.C., C.L., B.S., K.F., T.S., and S.S. performed research; A.T., S.D., M.C., C.L., B.S., K.F., T.S., S.S., M.L., and B.H. analyzed the data; C.G. and W.W. provided mutant mice and antibodies; F.B. supervised the research; A.T.,S.D., M.C., C.L., B.S., and F.B wrote the paper. T.S., S.S., B.J.H., C.G., and W.W. provided feedback and contributed to editing the manuscript.
These authors contributed equally.
AUTHOR CONTRIBUTIONS
OpenAccessLink https://www.cell.com/article/S0896627319306336/pdf
PMID 31400829
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SSID ssj0014591
Score 2.5847063
Snippet Injured axons fail to regenerate in the adult CNS, which contrasts with their vigorous growth during embryonic development. We explored the potential of...
SummaryInjured axons fail to regenerate in the adult CNS, which contrasts with their vigorous growth during embryonic development. We explored the potential of...
Injured axons fail to regenerate in the adult central nervous system, which contrasts their vigorous growth during embryonic development. We explored the...
SourceID pubmedcentral
proquest
crossref
pubmed
elsevier
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 1073
SubjectTerms Actin
actin dynamics
Actins - metabolism
ADF/cofilin
Animals
axon injury
axon regeneration
Axons
Axons - metabolism
Axons - pathology
Cofilin
Cofilin 1 - genetics
Cofilin 1 - metabolism
Cofilin 2 - genetics
Cofilin 2 - metabolism
conditioning
Destrin - genetics
Destrin - metabolism
Developmental plasticity
Embryogenesis
Genetic transformation
Growth Cones - metabolism
Growth Cones - pathology
Immunoglobulins
Intravital Microscopy
Mice
Microscopy
Microscopy, Confocal
Molecular modelling
Morphology
Nerve Regeneration - genetics
Neurons
Neurons - metabolism
Neurons - pathology
Rats
Regeneration
Spinal cord injuries
Spinal Cord Injuries - genetics
Spinal Cord Injuries - metabolism
Spinal Cord Injuries - pathology
Statistical analysis
Time-Lapse Imaging
Trauma
Variance analysis
Title ADF/Cofilin-Mediated Actin Turnover Promotes Axon Regeneration in the Adult CNS
URI https://dx.doi.org/10.1016/j.neuron.2019.07.007
https://www.ncbi.nlm.nih.gov/pubmed/31400829
https://www.proquest.com/docview/2297096092
https://search.proquest.com/docview/2272225447
https://pubmed.ncbi.nlm.nih.gov/PMC6763392
Volume 103
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