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Proteomic characterization of spontaneously regrowing spinal cord following injury in the teleost fish Apteronotus leptorhynchus, a regeneration-competent vertebrate

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Abstract

In adult mammals, spontaneous repair after spinal cord injury (SCI) is severely limited. By contrast, teleost fish successfully regenerate injured axons and produce new neurons from adult neural stem cells after SCI. The molecular mechanisms underlying this high regenerative capacity are largely unknown. The present study addresses this gap by examining the temporal dynamics of proteome changes in response to SCI in the brown ghost knifefish (Apteronotus leptorhynchus). Two-dimensional difference gel electrophoresis (2D DIGE) was combined with matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) and tandem mass spectrometry (MS/MS) to collect data during early (1 day), mid (10 days), and late (30 days) phases of regeneration following caudal amputation SCI. Forty-two unique proteins with significant differences in abundance between injured and intact control samples were identified. Correlation analysis uncovered six clusters of spots with similar expression patterns over time and strong conditional dependences, typically within functional families or between isoforms. Significantly regulated proteins were associated with axon development and regeneration; proliferation and morphogenesis; neuronal differentiation and re-establishment of neural connections; promotion of neuroprotection, redox homeostasis, and membrane repair; and metabolism or energy supply. Notably, at all three time points examined, significant regulation of proteins involved in inflammatory responses was absent.

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Data availability

Raw outputs from the Mascot search conducted as part of the protein identification analysis, including predicted masses, predicted sequences, and post-translational modifications for all matched peptides for the top ten databases matches for each protein spot selected for identification, are provided as Supplementary Information. Other data that support the findings of this study are available from the corresponding author upon reasonable request.

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Funding

This study was supported by the Ernst A.-C. Lange Stiftung, the Tönjes-Vagt-Stiftung, the National Science Foundation (contract grant number 1538505), and the Internationale Studien- und Ausbildungspartnerschaften (ISAP) program of the German Academic Exchange Service (DAAD).

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  1. Ruxandra F. Sîrbulescu

    Present address: Vaccine and Immunotherapy Center, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, 02129, USA

Authors and Affiliations

  1. School of Engineering and Science, Jacobs University Bremen, 28725, Bremen, Germany

    Ruxandra F. Sîrbulescu & Günther K. H. Zupanc

  2. School of Humanities and Social Sciences, Jacobs University Bremen, 28725, Bremen, Germany

    Iulian Ilieş

  3. Laboratory of Neurobiology, Department of Biology, Northeastern University, Boston, MA, 02115, USA

    Ruxandra F. Sîrbulescu, Iulian Ilieş, Lisa Amelung & Günther K. H. Zupanc

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  1. Ruxandra F. Sîrbulescu
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  2. Iulian Ilieş
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  4. Günther K. H. Zupanc
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Contributions

Study concept and design: GKHZ, RFS, II; conduction of experiments: RFS, LA; data analysis and interpretation: RFS, II, LA, GKHZ; writing of manuscript: GKHZ, RFS, II; preparation of figures: RFS, II; review and editing of manuscript: RFS, II, LA, GKHZ; coordination of study: GKHZ.

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Correspondence to Günther K. H. Zupanc.

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Sîrbulescu, R.F., Ilieş, I., Amelung, L. et al. Proteomic characterization of spontaneously regrowing spinal cord following injury in the teleost fish Apteronotus leptorhynchus, a regeneration-competent vertebrate. J Comp Physiol A 208, 671–706 (2022). https://doi.org/10.1007/s00359-022-01591-w

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