Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic
Tachykinins (TKs) are ancient neuropeptides present throughout the bilaterians and are, with some exceptions, characterized by a conserved FX1GX2Ramide carboxy terminus among protostomes and FXGLMamide in deuterostomes. The best-known TK is the vertebrate substance P, which in mammals, together with...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-11-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnins.2019.01262/full |
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| author | Dick R. Nässel Meet Zandawala Tsuyoshi Kawada Honoo Satake |
| author_facet | Dick R. Nässel Meet Zandawala Tsuyoshi Kawada Honoo Satake |
| author_sort | Dick R. Nässel |
| collection | DOAJ |
| description | Tachykinins (TKs) are ancient neuropeptides present throughout the bilaterians and are, with some exceptions, characterized by a conserved FX1GX2Ramide carboxy terminus among protostomes and FXGLMamide in deuterostomes. The best-known TK is the vertebrate substance P, which in mammals, together with other TKs, has been implicated in health and disease with important roles in pain, inflammation, cancer, depressive disorder, immune system, gut function, hematopoiesis, sensory processing, and hormone regulation. The invertebrate TKs are also known to have multiple functions in the central nervous system and intestine and these have been investigated in more detail in the fly Drosophila and some other arthropods. Here, we review the protostome and deuterostome organization and evolution of TK precursors, peptides and their receptors, as well as their functions, which appear to be partly conserved across Bilateria. We also outline the distribution of TKs in the brains of representative organisms. In Drosophila, recent studies have revealed roles of TKs in early olfactory processing, neuromodulation in circuits controlling locomotion and food search, nociception, aggression, metabolic stress, and hormone release. TK signaling also regulates lipid metabolism in the Drosophila intestine. In crustaceans, TK is an important neuromodulator in rhythm-generating motor circuits in the stomatogastric nervous system and a presynaptic modulator of photoreceptor cells. Several additional functional roles of invertebrate TKs can be inferred from their distribution in various brain circuits. In addition, there are a few interesting cases where invertebrate TKs are injected into prey animals as vasodilators from salivary glands or paralyzing agents from venom glands. In these cases, the peptides are produced in the glands of the predator with sequences mimicking the prey TKs. Lastly, the TK-signaling system appears to have duplicated in Panarthropoda (comprising arthropods, onychophores, and tardigrades) to give rise to a novel type of peptides, natalisins, with a distinct receptor. The distribution and functions of natalisins are distinct from the TKs. In general, it appears that TKs are widely distributed and act in circuits at short range as neuromodulators or cotransmitters. |
| first_indexed | 2024-12-13T21:51:43Z |
| format | Article |
| id | doaj.art-1ccc398d9cfc4f1e8e8112ffa547b9da |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-13T21:51:43Z |
| publishDate | 2019-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-1ccc398d9cfc4f1e8e8112ffa547b9da2022-12-21T23:30:14ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-11-011310.3389/fnins.2019.01262500979Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally PleiotropicDick R. Nässel0Meet Zandawala1Tsuyoshi Kawada2Honoo Satake3Department of Zoology, Stockholm University, Stockholm, SwedenDepartment of Neuroscience, Brown University, Providence, RI, United StatesBioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, JapanTachykinins (TKs) are ancient neuropeptides present throughout the bilaterians and are, with some exceptions, characterized by a conserved FX1GX2Ramide carboxy terminus among protostomes and FXGLMamide in deuterostomes. The best-known TK is the vertebrate substance P, which in mammals, together with other TKs, has been implicated in health and disease with important roles in pain, inflammation, cancer, depressive disorder, immune system, gut function, hematopoiesis, sensory processing, and hormone regulation. The invertebrate TKs are also known to have multiple functions in the central nervous system and intestine and these have been investigated in more detail in the fly Drosophila and some other arthropods. Here, we review the protostome and deuterostome organization and evolution of TK precursors, peptides and their receptors, as well as their functions, which appear to be partly conserved across Bilateria. We also outline the distribution of TKs in the brains of representative organisms. In Drosophila, recent studies have revealed roles of TKs in early olfactory processing, neuromodulation in circuits controlling locomotion and food search, nociception, aggression, metabolic stress, and hormone release. TK signaling also regulates lipid metabolism in the Drosophila intestine. In crustaceans, TK is an important neuromodulator in rhythm-generating motor circuits in the stomatogastric nervous system and a presynaptic modulator of photoreceptor cells. Several additional functional roles of invertebrate TKs can be inferred from their distribution in various brain circuits. In addition, there are a few interesting cases where invertebrate TKs are injected into prey animals as vasodilators from salivary glands or paralyzing agents from venom glands. In these cases, the peptides are produced in the glands of the predator with sequences mimicking the prey TKs. Lastly, the TK-signaling system appears to have duplicated in Panarthropoda (comprising arthropods, onychophores, and tardigrades) to give rise to a novel type of peptides, natalisins, with a distinct receptor. The distribution and functions of natalisins are distinct from the TKs. In general, it appears that TKs are widely distributed and act in circuits at short range as neuromodulators or cotransmitters.https://www.frontiersin.org/article/10.3389/fnins.2019.01262/fullsubstance Pneurokininneurokinin receptornatalisinG protein-coupled receptorco-transmission |
| spellingShingle | Dick R. Nässel Meet Zandawala Tsuyoshi Kawada Honoo Satake Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic Frontiers in Neuroscience substance P neurokinin neurokinin receptor natalisin G protein-coupled receptor co-transmission |
| title | Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic |
| title_full | Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic |
| title_fullStr | Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic |
| title_full_unstemmed | Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic |
| title_short | Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic |
| title_sort | tachykinins neuropeptides that are ancient diverse widespread and functionally pleiotropic |
| topic | substance P neurokinin neurokinin receptor natalisin G protein-coupled receptor co-transmission |
| url | https://www.frontiersin.org/article/10.3389/fnins.2019.01262/full |
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