Distribution of Brain-Derived Neurotrophic Factor in the Brain of the Small-Spotted Catshark <i>Scyliorhinus canicula,</i> and Evolution of Neurotrophins in Basal Vertebrates
Neurotrophins (NTFs) are structurally related neurotrophic factors essential for differentiation, survival, neurite outgrowth, and the plasticity of neurons. Abnormalities associated with neurotrophin-signaling (NTF-signaling) were associated with neuropathies, neurodegenerative disorders, and age-a...
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MDPI AG
2023-05-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/24/11/9495 |
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| author | Elena Chiavacci Sara Bagnoli Alessandro Cellerino Eva Terzibasi Tozzini |
| author_facet | Elena Chiavacci Sara Bagnoli Alessandro Cellerino Eva Terzibasi Tozzini |
| author_sort | Elena Chiavacci |
| collection | DOAJ |
| description | Neurotrophins (NTFs) are structurally related neurotrophic factors essential for differentiation, survival, neurite outgrowth, and the plasticity of neurons. Abnormalities associated with neurotrophin-signaling (NTF-signaling) were associated with neuropathies, neurodegenerative disorders, and age-associated cognitive decline. Among the neurotrophins, brain-derived neurotrophic factor (BDNF) has the highest expression and is expressed in mammals by specific cells throughout the brain, with particularly high expression in the hippocampus and cerebral cortex. Whole genome sequencing efforts showed that NTF signaling evolved before the evolution of Vertebrates; thus, the shared ancestor of Protostomes, Cyclostomes, and Deuterostomes must have possessed a single ortholog of neurotrophins. After the first round of whole genome duplication that occurred in the last common ancestor of Vertebrates, the presence of two neurotrophins in Agnatha was hypothesized, while the monophyletic group of cartilaginous fishes, or Chondrichthyans, was situated immediately after the second whole genome duplication round that occurred in the last common ancestor of Gnathostomes. Chondrichthyans represent the outgroup of all other living jawed vertebrates (Gnathostomes) and the sister group of Osteichthyans (comprehensive of Actinopterygians and Sarcopterygians). We were able to first identify the second neurotrophin in Agnatha. Secondly, we expanded our analysis to include the Chondrichthyans, with their strategic phylogenetic position as the most basal extant Gnathostome taxon. Results from the phylogenetic analysis confirmed the presence of four neurotrophins in the Chondrichthyans, namely the orthologs of the four mammalian neurotrophins BDNF, NGF, NT-3, and NT-4. We then proceeded to study the expression of BDNF in the adult brain of the Chondrichthyan <i>Scyliorhinus canicula</i>. Our results showed that BDNF is highly expressed in the <i>S. canicula</i> brain and that its expression is highest in the Telencephalon, while the Mesencephalic and Diencephalic areas showed expression of BDNF in isolated and well-defined cell groups. NGF was expressed at much lower levels that could be detected by PCR but not by in situ hybridization. Our results warrant further investigations in Chondrichthyans to characterize the putative ancestral function of neurotrophins in Vertebrates. |
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| issn | 1661-6596 1422-0067 |
| language | English |
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| spelling | doaj.art-3ecb62ab36cd4e5cb1c9d0a33a60ae262023-11-18T07:59:47ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-05-012411949510.3390/ijms24119495Distribution of Brain-Derived Neurotrophic Factor in the Brain of the Small-Spotted Catshark <i>Scyliorhinus canicula,</i> and Evolution of Neurotrophins in Basal VertebratesElena Chiavacci0Sara Bagnoli1Alessandro Cellerino2Eva Terzibasi Tozzini3Biology Laboratory (BIO@SNS), Scuola Normale Superiore, 56126 Pisa, ItalyBiology Laboratory (BIO@SNS), Scuola Normale Superiore, 56126 Pisa, ItalyBiology Laboratory (BIO@SNS), Scuola Normale Superiore, 56126 Pisa, ItalyBiology and Evolution of Marine Organisms Department (BEOM), Stazione Zoologica Anton Dohrn, 80121 Napoli, ItalyNeurotrophins (NTFs) are structurally related neurotrophic factors essential for differentiation, survival, neurite outgrowth, and the plasticity of neurons. Abnormalities associated with neurotrophin-signaling (NTF-signaling) were associated with neuropathies, neurodegenerative disorders, and age-associated cognitive decline. Among the neurotrophins, brain-derived neurotrophic factor (BDNF) has the highest expression and is expressed in mammals by specific cells throughout the brain, with particularly high expression in the hippocampus and cerebral cortex. Whole genome sequencing efforts showed that NTF signaling evolved before the evolution of Vertebrates; thus, the shared ancestor of Protostomes, Cyclostomes, and Deuterostomes must have possessed a single ortholog of neurotrophins. After the first round of whole genome duplication that occurred in the last common ancestor of Vertebrates, the presence of two neurotrophins in Agnatha was hypothesized, while the monophyletic group of cartilaginous fishes, or Chondrichthyans, was situated immediately after the second whole genome duplication round that occurred in the last common ancestor of Gnathostomes. Chondrichthyans represent the outgroup of all other living jawed vertebrates (Gnathostomes) and the sister group of Osteichthyans (comprehensive of Actinopterygians and Sarcopterygians). We were able to first identify the second neurotrophin in Agnatha. Secondly, we expanded our analysis to include the Chondrichthyans, with their strategic phylogenetic position as the most basal extant Gnathostome taxon. Results from the phylogenetic analysis confirmed the presence of four neurotrophins in the Chondrichthyans, namely the orthologs of the four mammalian neurotrophins BDNF, NGF, NT-3, and NT-4. We then proceeded to study the expression of BDNF in the adult brain of the Chondrichthyan <i>Scyliorhinus canicula</i>. Our results showed that BDNF is highly expressed in the <i>S. canicula</i> brain and that its expression is highest in the Telencephalon, while the Mesencephalic and Diencephalic areas showed expression of BDNF in isolated and well-defined cell groups. NGF was expressed at much lower levels that could be detected by PCR but not by in situ hybridization. Our results warrant further investigations in Chondrichthyans to characterize the putative ancestral function of neurotrophins in Vertebrates.https://www.mdpi.com/1422-0067/24/11/9495brain-derived neurotrophic factorBDNFneurotrophinssea lampreydogfishcatshark |
| spellingShingle | Elena Chiavacci Sara Bagnoli Alessandro Cellerino Eva Terzibasi Tozzini Distribution of Brain-Derived Neurotrophic Factor in the Brain of the Small-Spotted Catshark <i>Scyliorhinus canicula,</i> and Evolution of Neurotrophins in Basal Vertebrates International Journal of Molecular Sciences brain-derived neurotrophic factor BDNF neurotrophins sea lamprey dogfish catshark |
| title | Distribution of Brain-Derived Neurotrophic Factor in the Brain of the Small-Spotted Catshark <i>Scyliorhinus canicula,</i> and Evolution of Neurotrophins in Basal Vertebrates |
| title_full | Distribution of Brain-Derived Neurotrophic Factor in the Brain of the Small-Spotted Catshark <i>Scyliorhinus canicula,</i> and Evolution of Neurotrophins in Basal Vertebrates |
| title_fullStr | Distribution of Brain-Derived Neurotrophic Factor in the Brain of the Small-Spotted Catshark <i>Scyliorhinus canicula,</i> and Evolution of Neurotrophins in Basal Vertebrates |
| title_full_unstemmed | Distribution of Brain-Derived Neurotrophic Factor in the Brain of the Small-Spotted Catshark <i>Scyliorhinus canicula,</i> and Evolution of Neurotrophins in Basal Vertebrates |
| title_short | Distribution of Brain-Derived Neurotrophic Factor in the Brain of the Small-Spotted Catshark <i>Scyliorhinus canicula,</i> and Evolution of Neurotrophins in Basal Vertebrates |
| title_sort | distribution of brain derived neurotrophic factor in the brain of the small spotted catshark i scyliorhinus canicula i and evolution of neurotrophins in basal vertebrates |
| topic | brain-derived neurotrophic factor BDNF neurotrophins sea lamprey dogfish catshark |
| url | https://www.mdpi.com/1422-0067/24/11/9495 |
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