Distribution of NADPH‐diaphorase reactivity and effects of nitric oxide on feeding and locomotory circuitry in the pteropod mollusc, Clione limacina

Moroz, Leonid L.; Norekian, Tigran P.; Pirtle, Thomas J.; Robertson, Kirk J.; Satterlie, Richard A.

doi:10.1002/1096-9861(20001113)427:2<274::aid-cne8>3.3.co;2-r

Cited by 6 publications

(18 citation statements)

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“…Nitric oxide in molluscs plays a diversity of roles including control of neural functions with wide-spread expression both in ganglia and at the periphery (e.g. Moroz et al [2000]; Moroz [2006]; Moroz and Kohn [2011]). However, there is no reported detection of NO production by cells forming blood vessels in mollucs.…”

Section: Discussionmentioning

confidence: 99%

Molecular Evidence for Convergence and Parallelism in Evolution of Complex Brains of Cephalopod Molluscs: Insights from Visual Systems

Yoshida

Ogura

Ikeo

et al. 2015

Integrative and Comparative Biology

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Coleoid cephalopods show remarkable evolutionary convergence with vertebrates in their neural organization, including (1) eyes and visual system with optic lobes, (2) specialized parts of the brain controlling learning and memory, such as vertical lobes, and (3) unique vasculature supporting such complexity of the central nervous system. We performed deep sequencing of eye transcriptomes of pygmy squids (Idiosepius paradoxus) and chambered nautiluses (Nautilus pompilius) to decipher the molecular basis of convergent evolution in cephalopods. RNA-seq was complemented by in situ hybridization to localize the expression of selected genes. We found three types of genomic innovations in the evolution of complex brains: (1) recruitment of novel genes into morphogenetic pathways, (2) recombination of various coding and regulatory regions of different genes, often called "evolutionary tinkering" or "co-option", and (3) duplication and divergence of genes. Massive recruitment of novel genes occurred in the evolution of the "camera" eye from nautilus' "pinhole" eye. We also showed that the type-2 co-option of transcription factors played important roles in the evolution of the lens and visual neurons. In summary, the cephalopod convergent morphological evolution of the camera eyes was driven by a mosaic of all types of gene recruitments. In addition, our analysis revealed unexpected variations of squids' opsins, retinochromes, and arrestins, providing more detailed information, valuable for further research on intra-ocular and extra-ocular photoreception of the cephalopods.

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Section: Discussionmentioning

confidence: 99%

Molecular Evidence for Convergence and Parallelism in Evolution of Complex Brains of Cephalopod Molluscs: Insights from Visual Systems

Yoshida

Ogura

Ikeo

et al. 2015

Integrative and Comparative Biology

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“…In many ways, NOS systems in Pleurobranchaea are quite distinct from those described in Aplysia and Clione (see further), perhaps reflecting a role of feeding ecology in evolution of NO signaling, molluscan feeding, and defensive behaviors. 29,30,42 ■ SIGNIFICANCE OF NO-INDUCED pH i…”

Section: Acs Chemical Neurosciencementioning

confidence: 99%

cAMP, Ca²⁺, pH_i, and NO Regulate H-like Cation Channels That Underlie Feeding and Locomotion in the Predatory Sea Slug Pleurobranchaea californica

Green

Huang

Sudlow

et al. 2018

ACS Chem. Neurosci.

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A systems approach to regulation of neuronal excitation in the mollusc Pleurobranchaea has described novel interactions of cyclic AMP-gated cation current (I), Ca, pH, and NO. I appears in many neurons of feeding and locomotor neuronal networks. It is likely one of the family of hyperpolarization-activated, cyclic-nucleotide-gated currents (h-current) of vertebrate and invertebrate pacemaker networks. There are two isoforms. Ca regulates both voltage dependence and depolarization-sensitive inactivation in both isoforms. The Type 1 I of the feeding network is enhanced by intracellular acidification. A direct dependence of I on cAMP allows the current to be used as a reporter on cAMP concentrations in the cell, and from there to the intrinsic activities of the synthetic adenyl cyclase and the degradative phosphodiesterase. Type 2 I of the locomotor system is activated by serotonergic inputs, while Type 1 of the feeding network is thought to be regulated peptidergically. NO synthase activity is high in the CNS, where it differs from standard neuronal NO synthase in not being Ca sensitive. NO acidifies pH, potentiating Type 1, and may act to open proton channels. A cGMP pathway does not mediate NO effects as in other systems. Rather, nitrosylation likely mediates its actions. An integrated model of the action of cAMP, Ca, pH, and NO in the feeding network postulates that NO regulates proton conductance to cause neuronal excitation in the cell body on the one hand, and relief of activity-induced hyperacidification in fine dendritic processes on the other.

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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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116

139

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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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Distribution of NADPH‐diaphorase reactivity and effects of nitric oxide on feeding and locomotory circuitry in the pteropod mollusc, Clione limacina

Cited by 6 publications

References 0 publications

Molecular Evidence for Convergence and Parallelism in Evolution of Complex Brains of Cephalopod Molluscs: Insights from Visual Systems

Molecular Evidence for Convergence and Parallelism in Evolution of Complex Brains of Cephalopod Molluscs: Insights from Visual Systems

cAMP, Ca²⁺, pH_i, and NO Regulate H-like Cation Channels That Underlie Feeding and Locomotion in the Predatory Sea Slug Pleurobranchaea californica

Convergent evolution of neural systems in ctenophores

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Distribution of NADPH‐diaphorase reactivity and effects of nitric oxide on feeding and locomotory circuitry in the pteropod mollusc, Clione limacina

Cited by 6 publications

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Molecular Evidence for Convergence and Parallelism in Evolution of Complex Brains of Cephalopod Molluscs: Insights from Visual Systems

Molecular Evidence for Convergence and Parallelism in Evolution of Complex Brains of Cephalopod Molluscs: Insights from Visual Systems

cAMP, Ca2+, pHi, and NO Regulate H-like Cation Channels That Underlie Feeding and Locomotion in the Predatory Sea Slug Pleurobranchaea californica

Convergent evolution of neural systems in ctenophores

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cAMP, Ca²⁺, pH_i, and NO Regulate H-like Cation Channels That Underlie Feeding and Locomotion in the Predatory Sea Slug Pleurobranchaea californica