A Command Chemical Triggers an Innate Behavior by Sequential Activation of Multiple Peptidergic Ensembles

Kim, Young-Joon; Žitňan, Dušan; Galizia, C. Giovanni; Cho, Kook-Ho; Adams, Michael E.

doi:10.1016/j.cub.2006.06.027

Cited by 217 publications

(349 citation statements)

References 53 publications

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“…In related work, we have shown that ensembles of neurons in D. melanogaster homologous to those in M. sexta (EH-containing VM neurons, CCAP͞MIPs-containing IN704 neurons, and CCAP͞ bursicon-containing NS27 neurons) become active at the onset of successive behavioral subunits (15). Taken together, these findings indicate that sequential recruitment of peptidergic ensembles elicits components of an innate behavior in stepwise fashion.…”

Section: Recruitment Of Innate Behaviors By Peptidergic Networkmentioning

confidence: 65%

Central peptidergic ensembles associated with organization of an innate behavior

Kim

Žitňan

Cho³

et al. 2006

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

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168

158

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At the end of each developmental stage, insects perform the ecdysis sequence, an innate behavior necessary for shedding the old cuticle. Ecdysis triggering hormones (ETHs) initiate these behaviors through direct actions on the CNS. Here, we identify the ETH receptor (ETHR) gene in the moth Manduca sexta, which encodes two subtypes of GPCR (ETHR-A and ETHR-B). Expression of ETHRs in the CNS coincides precisely with acquisition of CNS sensitivity to ETHs and behavioral competence. ETHR-A occurs in diverse networks of neurons, producing both excitatory and inhibitory neuropeptides, which appear to be downstream signals for behavior regulation. These peptides include allatostatins, crustacean cardioactive peptide (CCAP), calcitonin-like diuretic hormone, CRF-like diuretic hormones (DHs) 41 and 30, eclosion hormone, kinins, myoinhibitory peptides (MIPs), neuropeptide F, and short neuropeptide F. In particular, cells L 3,4 in abdominal ganglia coexpress kinins, DH41, and DH30, which together elicit the fictive preecdysis rhythm. Neurons IN704 in abdominal ganglia coexpress CCAP and MIPs, whose joint actions initiate the ecdysis motor program. ETHR-A also is expressed in brain ventromedial cells, whose release of EH increases excitability in CCAP͞MIP neurons. These findings provide insights into how innate, centrally patterned behaviors can be orchestrated via recruitment of peptide cotransmitter neurons.ecdysis sequence ͉ ecdysis triggering hormone ͉ G protein-coupled receptors ͉ neuropeptide ͉ steroid I nnate behaviors are highly stereotypic and fully functional in the absence of prior experience. Examples include nurturing, nest building, courtship, and escape behaviors as well as certain developmental behaviors such as the ecdysis sequence, necessary for the shedding of old cuticle at the end of each developmental stage in insects. Because the ecdysis sequence is hormonally controlled, it provides unique opportunities to define mechanisms by which chemical messengers assemble and regulate the performance of behaviors (for review, see ref. 1).The ecdysis sequence is initiated through direct actions of bloodborne pre-ecdysis triggering hormone (PETH) and ecdysis triggering hormone (ETH) on the CNS (2, 3). These peptides are released from endocrine Inka cells, which are present throughout the Insecta (4-6). In larval Manduca sexta, the sequence consists of three behavioral phases (3). In the first phase, PETH activates preecdysis I behavior; subsequently, ETH activates preecdysis II and ecdysis behaviors. These behaviors can be elicited by ETH from the isolated CNS in vitro and, hence, are centrally patterned (3, 7).The ecdysis behavioral sequence is repeatedly acquired and lost throughout the life history of insects (3,8). The signaling pathways triggered by PETH and ETH are assembled at the end of each developmental stage through steroid-induced gene expression, which is critical for synthesis of PETH and ETH in Inka cells and sensitivity of the CNS to these peptides. Once ecdysis is performed, CNS sensitivity to ET...

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Section: Recruitment Of Innate Behaviors By Peptidergic Networkmentioning

confidence: 65%

Central peptidergic ensembles associated with organization of an innate behavior

Kim

Žitňan

Cho³

et al. 2006

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

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168

158

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“…3). These mutant SP and MIP1 peptides (SP [21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36] W23A,W32A , MIP1 W2A,W9A ) were completely inactive even in 10 μM concentration (Table 1), suggesting that these residues, and by inference the turn conformations, are critical for SPR activation. Furthermore, an MIP mutant (DmMIP1 3-8A ) carrying Ala-replacements in all residues except the conserved Trp residues retained a strong SPR agonist activity (Table 1).…”

mentioning

confidence: 99%

MIPs are ancestral ligands for the sex peptide receptor

Kim

Bartalska

Audsley

et al. 2010

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

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162

231

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Upon mating, females of many animal species undergo dramatic changes in their behavior. In Drosophila melanogaster, postmating behaviors are triggered by sex peptide (SP), which is produced in the male seminal fluid and transferred to female during copulation. SP modulates female behaviors via sex peptide receptor (SPR) located in a small subset of internal sensory neurons that innervate the female uterus and project to the CNS. Although required for postmating responses only in these female sensory neurons, SPR is expressed broadly in the CNS of both sexes. Moreover, SPR is also encoded in the genomes of insects that lack obvious SP orthologs. These observations suggest that SPR may have additional ligands and functions. Here, we identify myoinhibitory peptides (MIPs) as a second family of SPR ligands that is conserved across a wide range of invertebrate species. MIPs are potent agonists for Drosophila, Aedes, and Aplysia SPRs in vitro, yet are unable to trigger postmating responses in vivo. In contrast to SP, MIPs are not produced in male reproductive organs, and are not required for postmating behaviors in Drosophila females. We conclude that MIPs are evolutionarily conserved ligands for SPR, which are likely to mediate functions other than the regulation of female reproductive behaviors.Drosophila | female post-mating behavior | G protein-coupled receptor | neuropeptide | neuromodulation P eptide signaling through G protein-coupled receptors is a widely used mechanism for reversibly modulating the behavioral output of innate neural circuits (for review see ref. 1). A prominent example of peptidergic modulation of behavior is the regulation of female reproductive behavior in Drosophila melanogaster by the male's sex peptide (SP). SP is a small peptide present in the male seminal fluid. Upon mating, SP is transferred to the female, where it triggers dramatic changes in reproductive and other behaviors (2, 3). These behavioral modifications typically last for about a week, the period for which the female is able to store and use sperm from the initial mating (for review see ref. 4). Within females, SP is thought to activate a specific G protein-coupled receptor (SPR) (5) in a small set of internal sensory neurons of the female reproductive tract (6, 7). Signaling by SP and SPR is essential for the modulation of female behavior as these changes do not occur if the male lacks SP (8, 9) or the female lacks SPR (5).The modulation of female reproductive behavior in response to SP (and its closely related homolog DUP99B) (10, 11) is currently the only known role of SPR. Nonetheless, several lines of evidence have hinted that SPR may have other ligands and possibly also other functions. First, SPR is broadly expressed throughout the central nervous system (5), yet it is required only in reproductive tract sensory neurons for the postmating behavioral switch (6, 7). Second, SPR is also expressed in the central nervous system of males (5), where it is not likely to be exposed to SP. Third, orthologs of SPR are clearly d...

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“…59,60,[67][68][69][70] To truly understand the ecdysis behavior we have to examine the raison d'être of the molting process. Insects and crustaceans have a rigid exoskeleton and therefore to accommodate growth they have to periodically shed the exoskeleton and replace it with a new one.…”

Section: Ecdysis Motor Behavior Controlling Peptides: Ptth Eh Pethmentioning

confidence: 99%

“…The new cuticle is elaborated, sclerotized and hardened with the help of another neurohormone, bursicon (a 173 amino acid protein belonging to the cystine knot family of growth factors), which is coexpressed with CCAP in the bilateral ventral neurons in the central nervous system of Drosophila. 59,[67][68][69][70]73) The ecdysis cascade begins with the ventro-median cells (VM cells) secreting the eclosion hormone (EH) in the presence of 20E, which is stored in the proctodeal nerves (proct. nerve) which serves as the neurohemal organ and is released in the absence of 20E (Fig.…”

Section: Ecdysis Motor Behavior Controlling Peptides: Ptth Eh Pethmentioning

confidence: 99%

Molecular physiology of crustacean and insect neuropeptides

Mercier¹,

Doucet

Retnakaran³

2007

J. Pestic. Sci.

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One of the principal hallmarks of a living organism is its ability to respond to stimuli. As the unicellular organisms evolved into multicellular metazoans, the external signals perceived had to be transduced to several other cells requiring a neuronal network with its accompanying biochemical neurotransmitters. The progressive increase in complexity of the organisms necessitated the need for an integrated signal transducing system collecting external sensory stimuli and sending them to effector systems such that a dynamic equilibrium or homeostasis, which is essential for survival, could be maintained. During the course of evolution many advanced sense organs were developed to detect various parameters in the environment, and concomitantly different internal effector systems were formed to respond to these signals received from outside to maintain homeostasis. Coordination was achieved with a network of electrical conductors in the form of an arborized nervous system and a variety of hydrophilic biochemicals that acted as neurotransmitters carrying the sensory signals to the internal effector systems. As the animal became increasingly complex, a sophisticated neurotransmission system catering to the spatial and temporal needs during growth, development and reproduction had to be in place. Parts of the nervous tissue in many locations took on a secretory role and released protein signal transducers, the neuropeptides. A panoply of such neuropeptides exist in all organisms functioning as neurohormones, neurotransmitters or neuromodulators. Aspects of neuropeptide structure and function in insects and crustaceans have been reviewed by various authors. [1][2][3][4][5][6][7][8][9][10] The neuropeptides are ligands to their cognate receptors in the ef- Organisms have to constantly respond to environmental conditions to maintain a status of dynamic homeostasis for survival. As single celled organisms evolved into multicellular animals, intercellular and inter-organ communications became indispensable not only to orchestrate homeostasis but also to control the many events punctuating metazoan development. To accomplish this need, a signal transduction system was evolved, consisting of an arborized network of nerves as well as a collection of oligopeptide neurotransmitters (neuropeptides) along with their cognate receptors. We review here the current state of our understanding of the physiology of neuropeptides in the most species-rich group of animals, the crustaceans and insects. The vast majority of neuropeptides signal through cell-surface guanosine-protein coupled receptors (GPCRs). These neuropeptide-receptor systems control a variety of physiological functions, for instance the numerous involuntary movements of internal ducts that are precisely timed for transporting reproductive, digestive and secretory materials. The rigid exoskeleton in Crustaceans and Insects require periodic molts to accomplish growth and metamorphosis and this is harmoniously regulated by a cascade of neuropeptides. Neuropeptides also regul...

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A Command Chemical Triggers an Innate Behavior by Sequential Activation of Multiple Peptidergic Ensembles

Abstract: Our findings offer novel insights into how a command chemical orchestrates an innate behavior by stepwise recruitment of central peptidergic ensembles.

Cited by 217 publications

References 53 publications

Central peptidergic ensembles associated with organization of an innate behavior

Central peptidergic ensembles associated with organization of an innate behavior

MIPs are ancestral ligands for the sex peptide receptor

Molecular physiology of crustacean and insect neuropeptides

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