Localization of myoinhibitory peptide immunoreactivity in<i>Manduca sexta</i>and<i>Bombyx mori</i>, with indications that the peptide has a role in molting and ecdysis

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

Cho³

et al. 2006

168

158

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...

Section: In704 (Ccap and Mip)mentioning

confidence: 99%

Central peptidergic ensembles associated with organization of an innate behavior

Kim

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

Cho³

et al. 2006

168

158

“…In moths a network of 27/704 neurons produce neuropeptides CCAP and MIPs in abdominal ganglia Davis et al, 1993Davis et al, , 2003. The appearance of cGMP and decrease in CCAP-and MIP-immunohistochemical staining in axonal arborizations of 27/704 neurons indicates that these neuropeptides are released at ecdysis Davis et al, 2003).…”

Section: Roles Of Central Neuropeptides and Eth Receptors In Ecdysismentioning

confidence: 99%

“…The appearance of cGMP and decrease in CCAP-and MIP-immunohistochemical staining in axonal arborizations of 27/704 neurons indicates that these neuropeptides are released at ecdysis Davis et al, 2003). Incubation of the isolated CNS with CCAP alone results in ecdysis bursts in anterior abdominal ganglia Žitňan and Adams, 2000), whereas a mixture of CCAP and MIPs induces characteristic ecdysis burst patterns in the entire CNS (Kim et al, 2006a).…”

Section: Roles Of Central Neuropeptides and Eth Receptors In Ecdysismentioning

confidence: 99%

Complex steroid–peptide–receptor cascade controls insect ecdysis

General and Comparative Endocrinology

Kim

Žitňanová

et al. 2007

157

SUMMARYInsect ecdysis sequence is composed of pre-ecdysis, ecdysis and post-ecdysis behaviors controlled by a complex cascade of peptide hormones from endocrine Inka cells and neuropeptides in the central nervous system (CNS). Inka cells produce pre-ecdysis and ecdysis triggering hormones (ETH) which activate the ecdysis sequence through receptor-mediated actions on specific neurons in the CNS. Multiple experimental approaches have been used to determine mechanisms of ETH expression and release from Inka cells and its action on the CNS of moths and flies. During the preparatory phase 1-2 days prior to ecdysis, high ecdysteroid levels induce expression of ETH receptors in the CNS and increased ETH production in Inka cells, which coincides with expression of nuclear ecdysone receptor (EcR) and transcription factor cryptocephal (CRC). However, high ecdysteroid levels prevent ETH release from Inka cells. Acquisition of Inka cell competence to release ETH requires decline of ecdysteroid levels and β-FTZ-F1 expression few hours prior to ecdysis. The behavioral phase is initiated by ETH secretion into the hemolymph, which is controlled by two brain neuropeptides -corazonin and eclosion hormone (EH). Corazonin acts on its receptor in Inka cells to elicit low level ETH secretion and initiation of pre-ecdysis, while EH induces cGMP-mediated ETH depletion and consequent activation of ecdysis. The activation of both behaviors is accomplished by ETH action on central neurons expressing ETH receptors A and B (ETHR-A and B). These neurons produce numerous excitatory or inhibitory neuropeptides which initiate or terminate different phases of the ecdysis sequence. Our data indicate that insect ecdysis is a very complex process characterized by two principal steps: 1) Ecdysteroid-induced expression of receptors and transcription factors in the CNS and Inka cells. 2) Release and interaction of Inka cell peptide hormones and multiple central neuropeptides to control consecutive phases of the ecdysis sequence.

“…Closely related orthologs have since been identified in other species based on their inhibitory effects in various in vitro bioassays, such as the inhibition of juvenile hormone production in crickets (Lorenz et al, 1995a,b), the suppression of ecdysone secretion from prothoracic glands in the silk moth (Hua et al, 1999), and the inhibition of spontaneous peristaltic contractions of the adult M. sexta hindgut (Blackburn et al, 2001). Recently, it was proposed to act as a cotransmitter with other neuropeptides in the regulation of ecdysis behavior in M. sexta and D. melanogaster (Davis et al, 2003;Kim et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

Two novel neuropeptides in innervation of the salivary glands of the black‐legged tick, Ixodes scapularis: Myoinhibitory peptide and SIFamide

Šimo

J of Comparative Neurology

Park

2009

The peptidergic signaling system is an ancient cell-cell communication mechanism that is involved in numerous behavioral and physiological events in multicellular organisms. We identified two novel neuropeptides in the neuronal projections innervating the salivary glands of the blacklegged tick, Ixodes scapularis (Say, 1821). Myoinhibitory peptide (MIP) and SIFamide immunoreactivities were colocalized in the protocerebral cells and their projections terminating on specific cells of salivary gland acini (types II and III). Immunoreactive substances were identified by matrix-assisted laser desorption/ionization-time of flight (MALDITOF) analysis: a 1,321.6-Da peptide with the sequence typical for MIP (ASDWNRLSGMWamide) and a 1,395.7-Da SIFamide (AYRKPPFNGSIFamide), which are highly conserved among arthropods. Genes encoding these peptides were identified in the available Ixodes genome and expressed sequence tag (EST) database. In addition, the cDNA encoding the MIP prepropeptide was isolated by rapid amplification of cDNA ends (RACE). In this report, we describe the anatomical structure of specific central neurons innervating salivary gland acini and identify different neuropeptides and their precursors expressed by these neurons. Our data provide evidence for neural control of salivary gland by MIP and SIFamide from the synganglion, thus leading a basis for functional studies of these two distinct classes of neuropeptides. Keywords neuropeptide; myoinhibitory peptide; MIP; SIFamide; MALDI; synganglion; salivary glands Ticks are obligatory external parasites that feed on the blood of mammals, birds, and reptiles and often transmit pathogenic viruses, Rickettsiae, bacteria, and protozoa. Tick-borne diseases cause substantial economic loss in the animal industry and present risks for human health. The black-legged tick, Ixodes scapularis, transmits the most important tick-borne pathogen, Borrelia burgdorferi, which causes Lyme disease. More than 20,000 new cases are reported per year in the United States, in 46 states. This species also transmits other diseases, including human babesiosis Babesia microti and human granulocytic ehrlichiosis.Salivary secretions of ticks are essential during feeding for manipulation and suppression of host defense responses and might represent key components in the transmission of (Binnington, 1978;Coons and Roshdy, 1973;Krolak et al., 1982). Each type of acinus contains multiple cell types, including different types of secretory and epithelial cells (Balashov et al., 1983;Sauer et al., 1995;Sonenshine, 1993). Studies with transmission electron microscopy have discovered that axon terminals reach the basal region of the acini, indicating that there is neuronal control of the salivary glands (Balashov et al., 1983; Coons and Alberti, 1999). Recently, we have described the neuroanatomy of peptidergic cells in the nervous system, including the neurons and axonal projections that innervate tick salivary glands (Šimo et al., 2009).Previous immunohistochemical studies have indica...