A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc<i>Aplysia</i>

Wang, Huiying; Yu, Ke; Yang, Zhe; Zhang, Guo; Guo, Shi-Qi; Wang, Tao; Liu, Dandan; Jia, Ruonan; Zheng, Yu-Tong; Su, Yan-Nan; Liu, Yi; Weiss, Klaudiusz R.; Zhou, Haibo; Liu, Feng; Cropper, Elizabeth; Yu, Quan; Jing, Jian

doi:10.34133/research.0060

Cited by 4 publications

(3 citation statements)

References 77 publications

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“…Actually, the dysregulated REM sleep homeostatic timing including the SOREM sleep is indeed widely reported in narcolepsy [ 7 , 49 , 50 ]. It should also be noted that only SOREM sleep-like behavior, but not other kinds of disrupted timing such as cataplexy, occurs in the orexin SLD-caspase mice, even at the high REM sleep need condition, indicating that additional influences on the occurrence of cataplexy from other players may exist, such as the lack of orexin’s direct modulation on central motor excitation [ 36 , 51 – 53 ]. Observations from our high REM sleep need model help reveal more important characteristics of the orexin-SLD pathway for REM sleep homeostasis.…”

Section: Discussionmentioning

confidence: 99%

Orexin Neurons to Sublaterodorsal Tegmental Nucleus Pathway Prevents Sleep Onset REM Sleep-Like Behavior by Relieving the REM Sleep Pressure

Feng,

Qiao,

Luo

et al. 2024

Research

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Proper timing of vigilance states serves fundamental brain functions. Although disturbance of sleep onset rapid eye movement (SOREM) sleep is frequently reported after orexin deficiency, their causal relationship still remains elusive. Here, we further study a specific subgroup of orexin neurons with convergent projection to the REM sleep promoting sublaterodorsal tegmental nucleus (OX SLD neurons). Intriguingly, although OX SLD and other projection-labeled orexin neurons exhibit similar activity dynamics during REM sleep, only the activation level of OX SLD neurons exhibits a significant positive correlation with the post-inter-REM sleep interval duration, revealing an essential role for the orexin-sublaterodorsal tegmental nucleus (SLD) neural pathway in relieving REM sleep pressure. Monosynaptic tracing reveals that multiple inputs may help shape this REM sleep-related dynamics of OX SLD neurons. Genetic ablation further shows that the homeostatic architecture of sleep/wakefulness cycles, especially avoidance of SOREM sleep-like transition, is dependent on this activity. A positive correlation between the SOREM sleep occurrence probability and depression states of narcoleptic patients further demonstrates the possible significance of the orexin-SLD pathway on REM sleep homeostasis.

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Section: Discussionmentioning

confidence: 99%

Orexin Neurons to Sublaterodorsal Tegmental Nucleus Pathway Prevents Sleep Onset REM Sleep-Like Behavior by Relieving the REM Sleep Pressure

Feng,

Qiao,

Luo

et al. 2024

Research

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“…We sought to study an oxytocin/vasopressin signaling system in the gastropod mollusc Aplysia californica . Aplysia is an experimentally-advantageous system and has provided fundamental insight into the neural basis of motivated behaviors ( Jing and Weiss, 2002 ; Jing et al, 2004 ; Sasaki et al, 2009 ; Jing et al, 2010 ; Sasaki et al, 2013 ; Zhang et al, 2020 ; Bedecarrats et al, 2021 ; Evans et al, 2021 ; Due et al, 2022 ; Wang et al, 2023 ), learning and memory ( Sieling et al, 2014 ; Byrne and Hawkins, 2015 ; Orvis et al, 2022 ) and neuromodulation ( Cropper et al, 2018b ; Zhang et al, 2022 ), including neuropeptides ( Livnat et al, 2016 ; Zhang et al, 2017 ; Do et al, 2018 ; Zhang et al, 2018 ; Chan-Andersen et al, 2022 ) and receptors ( Bauknecht and Jekely, 2015 ; Checco et al, 2018 ; Guo et al, 2022 ; Jiang et al, 2022 ; Zhang et al, 2022 ). The first evidence for the presence of oxytocin/vasopressin-related neuropeptide in protostomes comes from an early immunohistochemical study ( Remy et al, 1979 ), and the later identification of an arginine vasopressin-like diuretic hormone ( Proux et al, 1987 ), both in insects.…”

Section: Introductionmentioning

confidence: 99%

Characterization of an Aplysia vasotocin signaling system and actions of posttranslational modifications and individual residues of the ligand on receptor activity

Ding

Guo

et al. 2023

Front. Pharmacol.

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The vasopressin/oxytocin signaling system is present in both protostomes and deuterostomes and plays various physiological roles. Although there were reports for both vasopressin-like peptides and receptors in mollusc Lymnaea and Octopus, no precursor or receptors have been described in mollusc Aplysia. Here, through bioinformatics, molecular and cellular biology, we identified both the precursor and two receptors for Aplysia vasopressin-like peptide, which we named Aplysia vasotocin (apVT). The precursor provides evidence for the exact sequence of apVT, which is identical to conopressin G from cone snail venom, and contains 9 amino acids, with two cysteines at position 1 and 6, similar to nearly all vasopressin-like peptides. Through inositol monophosphate (IP1) accumulation assay, we demonstrated that two of the three putative receptors we cloned from Aplysia cDNA are true receptors for apVT. We named the two receptors as apVTR1 and apVTR2. We then determined the roles of post-translational modifications (PTMs) of apVT, i.e., the disulfide bond between two cysteines and the C-terminal amidation on receptor activity. Both the disulfide bond and amidation were critical for the activation of the two receptors. Cross-activity with conopressin S, annetocin from an annelid, and vertebrate oxytocin showed that although all three ligands can activate both receptors, the potency of these peptides differed depending on their residue variations from apVT. We, therefore, tested the roles of each residue through alanine substitution and found that each substitution could reduce the potency of the peptide analog, and substitution of the residues within the disulfide bond tended to have a larger impact on receptor activity than the substitution of those outside the bond. Moreover, the two receptors had different sensitivities to the PTMs and single residue substitutions. Thus, we have characterized the Aplysia vasotocin signaling system and showed how the PTMs and individual residues in the ligand contributed to receptor activity.

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“…In the current work, we sought to characterize two Wamide neuropeptide signaling systems: GWa and MIP families, in a model system, mollusk Aplysia californica . Aplysia has emerged in recent years as a powerful lophotrochozoan/spiralians laboratory animal for the study of neuronal circuits, − motivated behaviors, ,− and neuromodulation. ,− …”

Section: Introductionmentioning

confidence: 99%

Molecular Characterization of Two Wamide Neuropeptide Signaling Systems in Mollusk Aplysia

Wang

Liu

et al. 2023

ACS Chem. Neurosci.

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Neuropeptides with the C-terminal Wamide (Trp-NH 2 ) are one of the last common ancestors of peptide families of eumetazoans and play various physiological roles. In this study, we sought to characterize the ancient Wamide peptides signaling systems in the marine mollusk Aplysia californica, i.e., APGWamide (APGWa) and myoinhibitory peptide (MIP)/Allatostatin B (AST-B) signaling systems. A common feature of protostome APGWa and MIP/AST-B peptides is the presence of a conserved Wamide motif in the C-terminus. Although orthologs of the APGWa and MIP signaling systems have been studied to various extents in annelids or other protostomes, no complete signaling systems have yet been characterized in mollusks. Here, through bioinformatics, molecular and cellular biology, we identified three receptors for APGWa, namely, APGWa-R1, APGWa-R2, and APGWa-R3. The EC 50 values for APGWa-R1, APGWa-R2, and APGWa-R3 are 45, 2100, and 2600 nM, respectively. For the MIP signaling system, we predicted 13 forms of peptides, i.e., MIP1−13 that could be generated from the precursor identified in our study, with MIP5 (WKQMAVWa) having the largest number of copies (4 copies). Then, a complete MIP receptor (MIPR) was identified and the MIP1−13 peptides activated the MIPR in a dose-dependent manner, with EC 50 values ranging from 40 to 3000 nM. Peptide analogs with alanine substitution experiments demonstrated that the Wamide motif at the C-terminus is necessary for receptor activity in both the APGWa and MIP systems. Moreover, cross-activity between the two signaling systems showed that MIP1, 4, 7, and 8 ligands could activate APGWa-R1 with a low potency (EC 50 values: 2800−22,000 nM), which further supported that the APGWa and MIP signaling systems are somewhat related. In summary, our successful characterization of Aplysia APGWa and MIP signaling systems represents the first example in mollusks and provides an important basis for further functional studies in this and other protostome species. Moreover, this study may be useful for elucidating and clarifying the evolutionary relationship between the two Wamide signaling systems (i.e., APGWa and MIP systems) and their other extended neuropeptide signaling systems.

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A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in MolluscAplysia

Cited by 4 publications

References 77 publications

Orexin Neurons to Sublaterodorsal Tegmental Nucleus Pathway Prevents Sleep Onset REM Sleep-Like Behavior by Relieving the REM Sleep Pressure

Orexin Neurons to Sublaterodorsal Tegmental Nucleus Pathway Prevents Sleep Onset REM Sleep-Like Behavior by Relieving the REM Sleep Pressure

Characterization of an Aplysia vasotocin signaling system and actions of posttranslational modifications and individual residues of the ligand on receptor activity

Molecular Characterization of Two Wamide Neuropeptide Signaling Systems in Mollusk Aplysia

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