Catecholaminergic System of Invertebrates: Comparative and Evolutionary Aspects in Comparison With the Octopaminergic System

Gallo, Valentina; Accordi, F.; Chimenti, C.; Civinini, Annalena; Crivellato, Enrico

doi:10.1016/bs.ircmb.2015.12.006

Cited by 28 publications

(26 citation statements)

References 120 publications

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“…As deuterostome invertebrates, echinoderms have always held a curious position with regards to neurotransmitter profiling. There is evidence that molecules traditionally reserved as being either invertebrate only (i.e., octopamine) or vertebrate only (i.e., norepinephrine) have been found in the echinoderm radial nerve ( 55 ), although there are higher levels of norepinephrine than octopamine ( 56 ). In the current study, we assume that the levels of tyramine and octopamine were too low for detection, or that they are rapidly metabolized during our tissue processing method.…”

Section: Resultsmentioning

confidence: 99%

Differences in Small Molecule Neurotransmitter Profiles From the Crown-of-Thorns Seastar Radial Nerve Revealed Between Sexes and Following Food-Deprivation

et al. 2018

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Neurotransmitters serve as chemical mediators of cell communication, and are known to have important roles in regulating numerous physiological and metabolic events in eumetazoans. The Crown-of-Thorns Seastar (COTS) is an asteroid echinoderm that has been the focus of numerous ecological studies due to its negative impact on coral reefs when in large numbers. Research devoted to its neural signaling, from basic anatomy to the key small neurotransmitters, would expand our current understanding of neural-driven biological processes, such as growth and reproduction, and offers a new approach to exploring the propensity for COTS population explosions and subsequent collapse. In this study we investigated the metabolomic profiles of small molecule neurotransmitters in the COTS radial nerve cord. Multivariate analysis shows differential abundance of small molecule neurotransmitters in male and female COTS, and in food-deprived individuals with significant differences between sexes in gamma-aminobutyric acid (GABA), histamine and serotonin, and significant differences in histamine and serotonin between satiation states. Annotation established that the majority of biosynthesis enzyme genes are present in the COTS genome. The spatial distribution of GABA, histamine and serotonin in the radial nerve cord was subsequently confirmed by immunolocalization; serotonin is most prominent within the ectoneural regions, including unique neural bulbs, while GABA and histamine localize primarily within neuropil fibers. Glutamic acid, which was also found in high relative abundance and is a precursor of GABA, is known as a spawning inhibitor in seastars, and as such was tested for inhibition of ovulation ex-vivo which resulted in complete inhibition of oocyte maturation and ovulation induced by 1-Methyladenine. These findings not only advance our knowledge of echinoderm neural signaling processes but also identify potential targets for developing novel approaches for COTS biocontrol.

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Section: Resultsmentioning

confidence: 99%

Differences in Small Molecule Neurotransmitter Profiles From the Crown-of-Thorns Seastar Radial Nerve Revealed Between Sexes and Following Food-Deprivation

et al. 2018

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“…The ubiquitous biogenic amines octopamine (OA), serotonin (5-HT) and dopamine (DA) activate neural circuitry to regulate behavior (Libersat and Pflueger, 2004 ; Bergan, 2015 ). The phylogenetic distribution of these neuromodulators suggests a deep evolutionary history predating the origin of the nervous system (Gallo et al, 2016 ). With few structural modifications, monoamines are functionally diverse in insects (Roeder, 1999 ; Mustard et al, 2005 ; Blenau and Thamm, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

Origins of Aminergic Regulation of Behavior in Complex Insect Social Systems

Kamhi

Arganda

Moreau

et al. 2017

Front. Syst. Neurosci.

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Neuromodulators are conserved across insect taxa, but how biogenic amines and their receptors in ancestral solitary forms have been co-opted to control behaviors in derived socially complex species is largely unknown. Here we explore patterns associated with the functions of octopamine (OA), serotonin (5-HT) and dopamine (DA) in solitary ancestral insects and their derived functions in eusocial ants, bees, wasps and termites. Synthesizing current findings that reveal potential ancestral roles of monoamines in insects, we identify physiological processes and conserved behaviors under aminergic control, consider how biogenic amines may have evolved to modulate complex social behavior, and present focal research areas that warrant further study.

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“…Octopamine (OA), an invertebrate biogenic amine, is similar to adrenalin and noradrenalin in its synthesis, its synthesizing enzymes, and the respective receptors; it is therefore suggested that adrenalin, noradrenalin, and OA derive from one ancestral pathway ( Gallo et al, 2016 ). Based on OA’s involvement in the fight-or-flight response, motivation, and aggression and it’s adipokinetic function in insects a similarity of function between OA in insects and the biogenic amines adrenalin and noradrenalin in vertebrates has been suggested (reviewed in Roeder, 2005 ).…”

Section: Introductionmentioning

confidence: 99%

Octopamine Underlies the Counter-Regulatory Response to a Glucose Deficit in Honeybees (Apis mellifera)

Buckemüller

Siehler

Göbel

et al. 2017

Front. Syst. Neurosci.

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An animal’s internal state is a critical parameter required for adaptation to a given environment. An important aspect of an animal’s internal state is the energy state that is adjusted to the needs of an animal by energy homeostasis. Glucose is one essential source of energy, especially for the brain. A shortage of glucose therefore triggers a complex response to restore the animal’s glucose supply. This counter-regulatory response to a glucose deficit includes metabolic responses like the mobilization of glucose from internal glucose stores and behavioral responses like increased foraging and a rapid intake of food. In mammals, the catecholamines adrenalin and noradrenalin take part in mediating these counter-regulatory responses to a glucose deficit. One candidate molecule that might play a role in these processes in insects is octopamine (OA). It is an invertebrate biogenic amine and has been suggested to derive from an ancestral pathway shared with adrenalin and noradrenalin. Thus, it could be hypothesized that OA plays a role in the insect’s counter-regulatory response to a glucose deficit. Here we tested this hypothesis in the honeybee (Apis mellifera), an insect that, as an adult, mainly feeds on carbohydrates and uses these as its main source of energy. We investigated alterations of the hemolymph glucose concentration, survival, and feeding behavior after starvation and examined the impact of OA on these processes in pharmacological experiments. We demonstrate an involvement of OA in these three processes in honeybees and conclude there is an involvement of OA in regulating a bee’s metabolic, physiological, and behavioral response following a phase of prolonged glucose deficit. Thus, OA in honeybees acts similarly to adrenalin and noradrenalin in mammals in regulating an animal’s counter-regulatory response.

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Catecholaminergic System of Invertebrates: Comparative and Evolutionary Aspects in Comparison With the Octopaminergic System

Cited by 28 publications

References 120 publications

Differences in Small Molecule Neurotransmitter Profiles From the Crown-of-Thorns Seastar Radial Nerve Revealed Between Sexes and Following Food-Deprivation

Differences in Small Molecule Neurotransmitter Profiles From the Crown-of-Thorns Seastar Radial Nerve Revealed Between Sexes and Following Food-Deprivation

Origins of Aminergic Regulation of Behavior in Complex Insect Social Systems

Octopamine Underlies the Counter-Regulatory Response to a Glucose Deficit in Honeybees (Apis mellifera)

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