Peptide Neuromodulation in Invertebrate Model Systems

Taghert, Paul H.; Nitabach, Michael N.

doi:10.1016/j.neuron.2012.08.035

Cited by 238 publications

(238 citation statements)

References 165 publications

(236 reference statements)

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“…One salient feature of neuropeptide modulation, common to both vertebrates and invertebrates, is their role in gating and controlling the gain of sensory inputs (51,52). Stress can trigger analgesia in mammals, a state whereby opioids signal to suppress the response of nociceptive neurons to aversive stimuli, and starvation induces an internal hunger state in flies, where increased dopamine signaling affects the sensitivity of taste neurons to sugar (52).…”

Section: Discussionmentioning

confidence: 99%

Molecular evolution of peptidergic signaling systems in bilaterians

Mirabeau

Joly

2013

Proc. Natl. Acad. Sci. U.S.A.

349

692

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Peptide hormones and their receptors are widespread in metazoans, but the knowledge we have of their evolutionary relationships remains unclear. Recently, accumulating genome sequences from many different species have offered the opportunity to reassess the relationships between protostomian and deuterostomian peptidergic systems (PSs). Here we used sequences of all human rhodopsin and secretin-type G protein-coupled receptors as bait to retrieve potential homologs in the genomes of 15 bilaterian species, including nonchordate deuterostomian and lophotrochozoan species. Our phylogenetic analysis of these receptors revealed 29 wellsupported subtrees containing mixed sets of protostomian and deuterostomian sequences. This indicated that many vertebrate and arthropod PSs that were previously thought to be phyla specific are in fact of bilaterian origin. By screening sequence databases for potential peptides, we then reconstructed entire bilaterian peptide families and showed that protostomian and deuterostomian peptides that are ligands of orthologous receptors displayed some similarity at the level of their primary sequence, suggesting an ancient coevolution between peptide and receptor genes. In addition to shedding light on the function of human G protein-coupled receptor PSs, this work presents orthology markers to study ancestral neuron types that were probably present in the last common bilaterian ancestor. neuropeptide evolution | GPCR evolution | bilaterian CNS cell types | bilaterian brain evolution

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Section: Discussionmentioning

confidence: 99%

Molecular evolution of peptidergic signaling systems in bilaterians

Mirabeau

Joly

2013

Proc. Natl. Acad. Sci. U.S.A.

349

692

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“…This article is a PNAS Direct Submission. 1 To whom correspondence should be addressed. E-mail: elevitan@pitt.edu.…”

Section: Significancementioning

confidence: 99%

“…However, there are also specialized neurons that have terminals that are packed with DCVs. Such neuroendocrine terminals are often linked to massive episodic neuropeptide release that triggers important behaviors such as egg laying in Aplysia or ecdysis in insects (1). The mechanism that accounts for variation in presynaptic neuropeptide storage (i.e., the number of DCVs in a terminal) in cotransmitting and neuroendocrine neurons remains unknown.…”

mentioning

confidence: 99%

Vesicle capture, not delivery, scales up neuropeptide storage in neuroendocrine terminals

Bulgari

Zhou

Hewes

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Neurons vary in their capacity to produce, store, and release neuropeptides packaged in dense-core vesicles (DCVs). Specifically, neurons used for cotransmission have terminals that contain few DCVs and many small synaptic vesicles, whereas neuroendocrine neuron terminals contain many DCVs. Although the mechanistic basis for presynaptic variation is unknown, past research demonstrated transcriptional control of neuropeptide synthesis suggesting that supply from the soma limits presynaptic neuropeptide accumulation. Here neuropeptide release is shown to scale with presynaptic neuropeptide stores in identified Drosophila cotransmitting and neuroendocrine terminals. However, the dramatic difference in DCV number in these terminals occurs with similar anterograde axonal transport and DCV half-lives. Thus, differences in presynaptic neuropeptide stores are not explained by DCV delivery from the soma or turnover. Instead, greater neuropeptide accumulation in neuroendocrine terminals is promoted by dramatically more efficient presynaptic DCV capture. Greater capture comes with tradeoffs, however, as fewer uncaptured DCVs are available to populate distal boutons and replenish neuropeptide stores following release. Finally, expression of the Dimmed transcription factor in cotransmitting neurons increases presynaptic DCV capture. Therefore, DCV capture in the terminal is genetically controlled and determines neuron-specific variation in peptidergic function.nerve terminal | secretory granule | neurotransmission | LDCV

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“…Evidence from many systems suggests that neuromodulators, such as biogenic amines or neuropeptides, are important regulators of internal states and behavior (Insel and Young 2000;Nassel and Winther 2010;Bargmann 2012;Marder 2012;Taghert and Nitabach 2012). As a first step toward understanding the neural coding of a state of aggressiveness, we carried out a screen for neuropeptide-secreting neurons that control agonistic behavior in Drosophila (Asahina et al 2014).…”

Section: A Neuron and A Neuropeptide That Control Aggressive Arousalmentioning

confidence: 99%

Internal States and Behavioral Decision-Making: Toward an Integration of Emotion and Cognition

Kennedy

Asahina²,

Hoopfer

et al. 2014

Cold Spring Harb Symp Quant Biol

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Social interactions, such as an aggressive encounter between two conspecific males or a mating encounter between a male and a female, typically progress from an initial appetitive or motivational phase, to a final consummatory phase. This progression involves both changes in the intensity of the animals' internal state of arousal or motivation and sequential changes in their behavior. How are these internal states, and their escalating intensity, encoded in the brain? Does this escalation drive the progression from the appetitive/motivational to the consummatory phase of a social interaction and, if so, how are appropriate behaviors chosen during this progression? Recent work on social behaviors in flies and mice suggests possible ways in which changes in internal state intensity during a social encounter may be encoded and coupled to appropriate behavioral decisions at appropriate phases of the interaction. These studies may have relevance to understanding how emotion states influence cognitive behavioral decisions at higher levels of brain function.

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Peptide Neuromodulation in Invertebrate Model Systems

Cited by 238 publications

References 165 publications

Molecular evolution of peptidergic signaling systems in bilaterians

Molecular evolution of peptidergic signaling systems in bilaterians

Vesicle capture, not delivery, scales up neuropeptide storage in neuroendocrine terminals

Internal States and Behavioral Decision-Making: Toward an Integration of Emotion and Cognition

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