Nitric oxide regulates swimming in the jellyfish <i>Aglantha digitale</i>

Moroz, Leonid L.; Meech, Robert W; Sweedler, Jonathan V.; Mackie, G. O.

doi:10.1002/cne.20023

Cited by 56 publications

(66 citation statements)

References 81 publications

(73 reference statements)

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“…Likewise, NADPHdiaphorase reactivity [a robust marker for nitric oxide synthase across cnidarians and other bilaterians (Moroz, 2006;Moroz et al, 2004;Moroz et al, 2000)] did not reveal specific fixative-resistant activity in Pleurobrachia.…”

Section: Reviewmentioning

confidence: 99%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

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117

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Neurons are defined as polarized secretory cells specializing in directional propagation of electrical signals leading to the release of extracellular messengers -features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. Multiple origins of neurons and synapses from different classes of ancestral secretory cells might have occurred more than once during ~600 million years of animal evolution with independent events of nervous system centralization from a common bilaterian/cnidarian ancestor without the bona fide central nervous system. Ctenophores, or comb jellies, represent an example of extensive parallel evolution in neural systems. First, recent genome analyses place ctenophores as a sister group to other animals. Second, ctenophores have a smaller complement of pan-animal genes controlling canonical neurogenic, synaptic, muscle and immune systems, and developmental pathways than most other metazoans. However, comb jellies are carnivorous marine animals with a complex neuromuscular organization and sophisticated patterns of behavior. To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organization of integrative and locomotory systems. Third, many bilaterian/cnidarian neuron-specific genes and 'classical' neurotransmitter pathways are either absent or, if present, not expressed in ctenophore neurons (e.g. the bilaterian/cnidarian neurotransmitter, γ-amino butyric acid or GABA, is localized in muscles and presumed bilaterian neuronspecific RNA-binding protein Elav is found in non-neuronal cells). Finally, metabolomic and pharmacological data failed to detect either the presence or any physiological action of serotonin, dopamine, noradrenaline, adrenaline, octopamine, acetylcholine or histamineconsistent with the hypothesis that ctenophore neural systems evolved independently from those in other animals. Glutamate and a diverse range of secretory peptides are first candidates for ctenophore neurotransmitters. Nevertheless, it is expected that other classes of signal and neurogenic molecules would be discovered in ctenophores as the next step to decipher one of the most distinct types of neural organization in the animal kingdom.

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Section: Reviewmentioning

confidence: 99%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

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117

139

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“…The modulatory effects of NO on a variety of neuronal circuits across different phyla have been described. NO affects rhythmic motor activity in jellyfish swimming (Moroz et al, 2004), snail feeding (Kobayashi et al, 2000), and cardiac activity (Taylor et al, 2003), crab stomatogastric activity (Scholz et al, 2001;Stein et al, 2005), locust oviposition (Newland and Yates, 2007), and mouthpart movements (Rast, 2001), frog respiration (Hedrick and Morales, 1999), tadpole swimming (McLean and Sillar, 2000), lamprey swimming (Kyriakatos and El Manira, 2007), and mammalian respiration (Pierrefiche et al, 2007;Reeves et al, 2008). The mechanisms NO uses to exert its effects are less well known, with a notable exception being in the tadpole spinal cord Sillar, 2002, 2004).…”

Section: Discussionmentioning

confidence: 99%

The Nitric Oxide/cGMP Pathway Tunes the Thermosensitivity of Swimming Motor Patterns inXenopus laevisTadpoles

Robertson

Sillar²

2009

J. Neurosci.

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We investigated the role of the nitric oxide (NO)/cGMP pathway in setting thresholds for failure and recovery during hyperthermic stress of the swimming central pattern generator of immobilized Xenopus tadpoles (stage 42). We recorded swimming motor patterns induced by tail skin stimulation (TS) (1 ms current pulse) or by bath application of 50 M NMDA. Swimming rhythm frequency increased in a linear manner with increasing temperature. In the presence of the NO donor S-nitroso-N-acetylpenicillamine (SNAP), recovery from hyperthermic failure was greatly slowed, often taking longer than the duration of the experiment. Pharmacological activation of the NO/cGMP pathway using SNAP or 8-bromo-cGMP (1) decreased the duration of TS-evoked swim episodes; (2) decreased the temperature threshold for hyperthermic circuit failure; (3) decreased the temperature at which the circuit recovered; and (4) increased the time taken to recover. Pharmacological inhibition of the NO/cGMP pathway using the NO scavenger CPTIO, the nitric oxide synthase (NOS) inhibitor L-NAME or the guanylyl cyclase inhibitor ODQ (1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one) had the opposite effects. NMDA rhythms were more resistant to hyperthermic failure than TS-evoked swim episodes, but the effects of SNAP on the temperature sensitivity of swimming evoked by NMDA were similar to those on TS-evoked swimming, suggesting that drug effects occur on central patterngenerating networks rather than sensory pathways. We conclude that the NO/cGMP pathway is involved in setting the threshold temperatures for hyperthermic failure and subsequent recovery of fictive swimming in tadpoles, and we suggest that this is part of a variable response to prevent overexcitation during abiotic stress under different environmental conditions.

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“…Some axons projecting from nerve 1 of the abdominal ganglia are immunopositive (H. Aonuma, personal communication). An NO-cGMP pathway has been widely reported in many sensory and motor systems in both vertebrates and invertebrates (Bawin et al, 1994;Bicker and Schmachtenberg, 1997;Araki et al, 2004;Moroz et al, 2004;Newland and Yates, 2007). Newland and Yates (Newland and Yates, 2007) show that bath application of the generic protein kinase inhibitor H-7 and a selective cGMP-dependent protein kinase (PKG) inhibitor KT-5823 reduced the frequency of the oviposition digging rhythm of the locust.…”

Section: Research Articlementioning

confidence: 97%

“…NO inhibits the swimming rhythm of Xenopus laevis tadpoles (McLean and Sillar, 2002), suppresses a feeding response of the pond snail (Kobayashi et al, 2000) and decreases the heartbeat frequency in the lobster (Mahadevan et al, 2004). By contrast, NO is also reported to increase respiratory rhythm of the bullfrog (Hedrick and Morales, 1999), the swimming frequency of jellyfish (Moroz et al, 2004) and the oviposition digging rhythm of locusts (Newland and Yates, 2007).…”

Section: Introductionmentioning

confidence: 98%

Nitric oxide modulates a swimmeret beating rhythm in the crayfish

Mita

Yoshida

Nagayama

2014

Journal of Experimental Biology

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The modulatory effects of nitric oxide (NO) and cAMP on the rhythmic beating activity of the swimmeret motor neurones in the crayfish were examined. Swimmerets are paired appendages located on the ventral side of each abdominal segment that show rhythmic beating activity during forward swimming, postural righting behaviour and egg ventilation in gravid females. In isolated abdominal nerve cord preparations, swimmeret motor neurones are usually silent or show a continuous low-frequency spiking activity. Application of carbachol, a cholinergic agonist, elicited rhythmic bursts of motor neurone spikes. The co-application of L-arginine, the substrate for NO synthesis with carbachol increased the burst frequency of the motor neurones. The co-application of the NO donor SNAP with carbachol also increased the burst frequency of the motor neurones. By contrast, co-application of a NOS inhibitor, L-NAME, with carbachol decreased beating frequency of the motor neurones. These results indicate that NO may act as a neuromodulator to facilitate swimmeret beating activity. The facilitatory effect of L-arginine was cancelled by co-application of the soluble guanylate cyclase (sGC) inhibitor ODQ suggesting that NO acts by activating sGC to promote the production of cGMP. Application of L-arginine alone or membrane-permeable cGMP analogue 8-Br-cGMP alone did not elicit rhythmic activity of motor neurones, but co-application of 8-Br-cGMP with carbachol increased bursting frequency of the motor neurones. Furthermore, application of the membrane-permeable cAMP analogue CPT-cAMP alone produced rhythmic bursting of swimmeret motor neurones, and the bursting frequency elicited by CPT-cAMP was increased by coapplication with L-arginine. Co-application of the adenylate cyclase inhibitor SQ22536 ceased rhythmic bursts of motor neurone spikes elicited by carbachol. These results suggest that a cAMP system enables the rhythmic bursts of motor neurone spikes and that a NO-cGMP signaling pathway increases cAMP activity to facilitate swimmeret beating.

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Nitric oxide regulates swimming in the jellyfish Aglantha digitale

Cited by 56 publications

References 81 publications

Convergent evolution of neural systems in ctenophores

Convergent evolution of neural systems in ctenophores

The Nitric Oxide/cGMP Pathway Tunes the Thermosensitivity of Swimming Motor Patterns inXenopus laevisTadpoles

Nitric oxide modulates a swimmeret beating rhythm in the crayfish

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