Phenotypic maturation of neurons and continuous precursor migration in the formation of the peduncle nerve net in Hydra
Open accessAbstract
Mechanisms of nerve net formation in Hydra were analyzed using a monoclonal antibody (L96) directed against neurons of the peduncle, the basal end of the polyp's body axis. L96+ neurons express RFamide neuropeptides and constitute 70-80% of all ectodermal neurons in the lower peduncle. L96+ neurons arise from neuronal precursors which immigrate from the gastric region into the upper peduncle and first differentiate into neurons lacking the L96 antigen. By tissue movement, these L96- neurons become displaced to the lower peduncle where L96 antigen expression is initiated. The entire L96 neuron differentiation pathway requires about 4 days, but regeneration stimuli shorten it to only 36 hr. Our experiments indicate that local extrinsic signals released by epithelial cells in the peduncle control the L96+ neuron differentiation pathway. Ectopic L96+ neuron differentiation can be induced by LiCl treatment, which also stimulates ectopic feet in the gastric region. Further experiments show that intrinsic signals are also involved in the L96+ neuron differentiation pathway. Neurons of the gastric region become continuously displaced to the peduncle by tissue movement, but these "old" neurons fail to express the L96 antigen in response to the altered epithelial environment. Gastric neurons also fail to express the L96 antigen after LiCl treatment or regeneration in stem cell-depleted polyps. Thus, the competence of neurons to respond to environmental cues with L96 antigen expression is strongly age-dependent. We define this age-dependent acquisition of the neuronal phenotype as phenotypic maturation controlled by the target tissue.
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In Hydra, regeneration neurogenesis is accomplished by integrating stem cell derived migratory neuronal precursor cells into the nervous system.
“In Hydra, this is accomplished by integrating stem cell derived migratory neuronal precursor cells into the nervous system [95,96].”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [96]
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“After entering the neuron differentiation pathway, about a half of the neuron precursor cells migrate toward the head or the foot (Heimfeld and Bode 1984; Fujisawa 1989; Teragawa and Bode 1990, 1995; Technau and Holstein 1996; Hager and David 1997).”
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Self-citationChapter 3 Stem Cells in Immortal Hydra
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- Authors
- Technau, U., & Holstein, T. W.
- Affiliations
- Goethe University Frankfurt (DE)
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 1996-08
- Volume
- 177
- Issue
- 2
- Pages
- 599-615
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2078870439
- Cited by
- 49
- References
- 0
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 3 · 2022: 3 · 2019: 3 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 2 · 2012: 3
- FWCI
- 3.21
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- Hydra, peduncle, neuronal precursors, neuronal differentiation, tissue movement, regeneration, stem cell depletion
- MeSH terms
- Animals, Antibodies, Monoclonal, Cell Differentiation, Cell Movement, Hydra, Nerve Net, Nerve Tissue Proteins, Neurons, Phenotype, Stem Cells
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