Characterization of<i>NvLWamide-like</i>neurons reveals stereotypy in<i>Nematostella</i>nerve net development

Havrilak, Jamie A.; Faltine-Gonzalez, Dylan Z.; Wen, Yiling; Fodera, Daniella; Simpson, Ayanna C.; Magie, Craig R.; Layden, Michael J.

doi:10.1101/145623

Cited by 2 publications

(2 citation statements)

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“…1H). This is consistent with our previous observations that juvenile polyp nervous systems resemble adult nervous systems, but have fewer total neurons [41]. We conclude that acetylcholine induces tentacular contractions in N. vectensis, which is similar to observed responses in other cnidarians (Reviewed in [46].…”

Section: Resultssupporting

confidence: 92%

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Characterization of nAChRs in Nematostella vectensis supports neuronal and non-neuronal roles in the cnidarian–bilaterian common ancestor

Faltine-Gonzalez¹,

Layden²

2019

EvoDevo

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BackgroundNicotinic and muscarinic acetylcholine receptors likely evolved in the cnidarian–bilaterian common ancestor. Both receptor families are best known for their role at chemical synapses in bilaterian animals, but they also have described roles as non-neuronal signaling receptors within the bilaterians. It is not clear when either of the functions for nicotinic or muscarinic receptors evolved. Previous studies in cnidarians suggest that acetylcholine’s neuronal role existed prior to the cnidarian–bilaterian divergence, but did not address potential non-neuronal functions. To determine the origins of neuronal and non-neuronal functions of nicotinic acetylcholine receptors, we investigated the phylogenetic position of cnidarian acetylcholine receptors, characterized the spatiotemporal expression patterns of nicotinic receptors in N. vectensis, and compared pharmacological studies in N. vectensis to the previous work in other cnidarians.ResultsConsistent with described activity in other cnidarians, treatment with acetylcholine-induced tentacular contractions in the cnidarian sea anemone N. vectensis. Phylogenetic analysis suggests that the N. vectensis genome encodes 26 nicotinic (nAChRs) and no muscarinic (mAChRs) acetylcholine receptors and that nAChRs independently radiated in cnidarian and bilaterian linages. The namesake nAChR agonist, nicotine, induced tentacular contractions similar to those observed with acetylcholine, and the nAChR antagonist mecamylamine suppressed tentacular contractions induced by both acetylcholine and nicotine. This indicated that tentacle contractions are in fact mediated by nAChRs. Nicotine also induced the contraction of radial muscles, which contract as part of the peristaltic waves that propagate along the oral–aboral axis of the trunk. Radial contractions and peristaltic waves were suppressed by mecamylamine. The ability of nicotine to mimic acetylcholine responses, and of mecamylamine to suppress acetylcholine and nicotine-induced contractions, supports a neuronal function for acetylcholine in cnidarians. Examination of the spatiotemporal expression of N. vectensis nAChRs (NvnAChRs) during development and in juvenile polyps identified that NvnAChRs are expressed in neurons, muscles, gonads, and large domains known to be consistent with a role in developmental patterning. These patterns are consistent with nAChRs functioning in both a neuronal and non-neuronal capacity in N. vectensis.ConclusionOur data suggest that nAChR receptors functioned at chemical synapses in N. vectensis to regulate tentacle contraction. Similar responses to acetylcholine are well documented in cnidarians, suggesting that the neuronal function represents an ancestral role for nAChRs. Expression patterns of nAChRs are consistent with both neuronal and non-neuronal roles for acetylcholine in cnidarians. Together, these observations suggest that both neuronal and non-neuronal functions for the ancestral nAChRs were present in the cnidarian–bilaterian common ancestor. Thus, both roles described in bilate...

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Section: Resultssupporting

confidence: 92%

“…Each gene was sub-cloned into pGEM-T (Promega) from mixed stage cDNA using the primers listed in Additional file 4: Table S1. Embryo fixation, RNA probe synthesis, in situ hybridization, and immunohistochemistry protocols were performed as previously described [41, 42]. Juvenile polyps were fixed for 2 h as previously described [43].…”

Section: Methodsmentioning

confidence: 99%

Characterization of nAChRs in Nematostella vectensis supports neuronal and non-neuronal roles in the cnidarian–bilaterian common ancestor

Faltine-Gonzalez¹,

Layden²

2019

EvoDevo

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Dynamics and variability of neuronal subtype responses during growth, degrowth, and regeneration

Havrilak

Al-Shaer

Baban

et al. 2019

Preprint

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32The cell dynamics and responses of individual neuronal cell types during whole-33 body axis regeneration are not well understood in any system. We exploited transgenic 34 technology to track individual neuronal subtypes within regenerating Nematostella 35 vectensis nerve nets in vivo. Individual neuronal subtypes had specific responses that 36 included always, never, and conditional regeneration. Regenerates were smaller than the 37 pre-amputated animal, and the nerve net was reduced in neuronal number. The reduced 38 nerve net in regenerates led us to investigate whether the nerve net scaled with changes in 39 body size. Neuronal number decreased as animals shrunk in response to starvation. 40Conversely, neurons increased in fed animals as they increased in length. The increase 41 and decrease of neurons was reversible by switching fed animals to starvation and vice 42 versa. Regenerates and starved/fed animals with scaled-down or scaled-up nervous 43 systems responded to external mechanical cues. These data suggest that the Nematostella 44 nerve net is dynamic, capable of scaling with changes to overall body size, and that 45 individual neuronal subtypes display differential regenerative potential which is likely 46 linked to the scale-state of regenerating nervous system. 47 studies aimed at understanding the molecular mechanisms that re-pattern whole nervous 63 systems. 64

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Characterization ofNvLWamide-likeneurons reveals stereotypy inNematostellanerve net development

Cited by 2 publications

References 40 publications

Characterization of nAChRs in Nematostella vectensis supports neuronal and non-neuronal roles in the cnidarian–bilaterian common ancestor

Characterization of nAChRs in Nematostella vectensis supports neuronal and non-neuronal roles in the cnidarian–bilaterian common ancestor

Dynamics and variability of neuronal subtype responses during growth, degrowth, and regeneration

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