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Central nervous system regeneration in ascidians: cell migration and differentiation

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Abstract

Adult ascidians have the capacity to regenerate the central nervous system (CNS) and are therefore excellent models for studies on neuroregeneration. The possibility that undifferentiated blood cells are involved in adult neuroregeneration merits investigation. We analyzed the migration, circulation, and role of hemocytes of the ascidian Styela plicata in neuroregeneration. Hemocytes were removed and incubated with superparamagnetic iron oxide nanoparticles (SPION), and these SPION-labeled hemocytes were injected back into the animals (autologous transplant), followed by neurodegeneration with the neurotoxin 3-acetylpyridine (3AP). Magnetic resonance imaging showed that 1, 5, and 10 days after injury, hemocytes migrated to the intestinal region, siphons, and CNS. Immunohistochemistry revealed that the hemocytes that migrated to the CNS were putative stem cells (P-element-induced wimpy testis + or PIWI + cells). In the cortex of the neural ganglion, migrated hemocytes started to lose their PIWI labeling 5 days after injury, and 10 days later started to show β-III tubulin labeling. In the neural gland, however, the hemocytes remained undifferentiated during the entire experimental period. Transmission electron microscopy revealed regions in the neural gland with characteristics of neurogenic niches, not previously reported in ascidians. These results showed that migration of hemocytes to the hematopoietic tissue and to the 3AP-neurodegenerated region is central to the complex mechanism of neuroregeneration.

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Acknowledgements

We are grateful to Auriane Cassan Rémond for the schemes and to Rosalia Mendez-Otero for providing the nanoparticles. Janet W. Reid (JWR Associates, New York, USA) revised the English.

Funding

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil), and Fundação Carlos Chagas Filho de Apoio à Pesquisa do Estado do Rio de Janeiro (FAPERJ/RJ/Brazil) to ISA, IJRW, SA and CMB. The authors are indebted to the Plataforma de Microscopia Eletrônica Rudolph Barth from the Instituto Oswaldo Cruz/Fiocruz and to the Centro Nacional de Biologia Estrutural e Bioimagem from the Universidade Federal do Rio de Janeiro.

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  1. Silvana Allodi and Cintia Monteiro-de-Barros contributed equally to the work.

Authors and Affiliations

  1. Laboratório de Neurobiologia Comparativa e do Desenvolvimento, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, RJ, 21949-902, Rio de Janeiro, Brazil

    Isadora Santos de Abreu, Inês Júlia Ribas Wajsenzon & Silvana Allodi

  2. Programa de Pós-Graduação em Ciências Biológicas – Fisiologia, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro – UFRJ, Av. Carlos Chagas Filho 373, Ilha do Fundão, 21949-902, RJ, 21949-902, Rio de Janeiro, Brazil

    Isadora Santos de Abreu & Silvana Allodi

  3. Departamento de Morfologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil

    José Correa Dias Jr.

  4. Laboratório Integrado de Biociências Translacionais, Instituto de Biodiversidade e Sustentabilidade – NUPEM, Universidade Federal do Rio de Janeiro, Av. São José do Barreto, 764, São José do Barreto, Macaé, RJ, 27965-045, Brazil

    Cintia Monteiro-de-Barros

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  1. Isadora Santos de Abreu
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  3. José Correa Dias Jr.
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  4. Silvana Allodi
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  5. Cintia Monteiro-de-Barros
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Contributions

ISA, SA, and CMB conceived and designed the study. ISA, IJRW, and JDCJr performed the experiments. ISA, JDC Jr, SA, and CMB conducted the analyses. ISA, SA, and CMB wrote the manuscript. All the authors read and approved the final manuscript.

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Correspondence to Silvana Allodi or Cintia Monteiro-de-Barros.

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441_2022_3677_MOESM1_ESM.tif

Supplementary file1 Fig. 1. MRI of control animals (injected only with sea water). The ascidians show a faint signal in the intestine (white arrow) and gonads (black arrowheads) (TIF 368 KB)

Supplementary file2 Fig. 2. Styela plicata blood cell viability after in-vitro incubation with SPION (DOCX 14 KB)

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de Abreu, I.S., Wajsenzon, I.J.R., Dias, J.C. et al. Central nervous system regeneration in ascidians: cell migration and differentiation. Cell Tissue Res 390, 335–354 (2022). https://doi.org/10.1007/s00441-022-03677-y

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