Identification of a new member of the GLWamide peptide family: physiological activity and cellular localization in cnidarian polyps

Takahashi, Toshio; Kobayakawa, Yoshitaka; Muneoka, Yojiro; Fujisawa, Yuko; Mohri, Satoshi; Hatta, Masayuki; Shimizu, Hiroshi; Fujisawa, Toshitaka; Sugiyama, T.; Takahara, Masakazu; Yanagi, Kensuke; Koizumi, Osamu

doi:10.1016/s1096-4959(03)00088-5

Cited by 50 publications

(63 citation statements)

References 30 publications

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“…Neuropeptides Hym-53, Hym-355 and CGLW amide trigger the oocyte maturation and spawning in hydrozoan jellyfish (Takeda et al, 2013). The GLW amide was shown earlier to have a role in muscle contraction and metamorphosis in Hydra (Takahashi et al, 2003). Similarly, another neuropeptide, Hym-176, induces ectodermal muscle contraction in Hydra (Yum et al, 1998).…”

Section: N V E C T E N S I S T a D H A E R E N S A Q U E E N S mentioning

confidence: 99%

The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system

Krishnan

Schiöth

2015

Journal of Experimental Biology

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The origin and evolution of the nervous system is one of the most intriguing and enigmatic events in biology. The recent sequencing of complete genomes from early metazoan organisms provides a new platform to study the origins of neuronal gene families. This review explores the early metazoan expansion of the largest integral transmembrane protein family, the G protein-coupled receptors (GPCRs), which serve as molecular targets for a large subset of neurotransmitters and neuropeptides in higher animals. GPCR repertories from four pre-bilaterian metazoan genomes were compared. This includes the cnidarian Nematostella vectensis and the ctenophore Mnemiopsis leidyi, which have primitive nervous systems (nerve nets), the demosponge Amphimedon queenslandica and the placozoan Trichoplax adhaerens, which lack nerve and muscle cells. Comparative genomics demonstrate that the rhodopsin and glutamate receptor families, known to be involved in neurotransmission in higher animals are also widely found in prebilaterian metazoans and possess substantial expansions of rhodopsin-family-like GPCRs. Furthermore, the emerging knowledge on the functions of adhesion GPCRs in the vertebrate nervous system provides a platform to examine possible analogous roles of their closest homologues in pre-bilaterians. Intriguingly, the presence of molecular components required for GPCR-mediated neurotransmission in pre-bilaterians reveals that they exist in both primitive nervous systems and nerve-cell-free environments, providing essential comparative models to better understand the origins of the nervous system and neurotransmission. KEY WORDS: Neuron, GPCR, Nerve net, Synapse, EvolutionIntroduction G protein-coupled receptors (GPCRs) constitute the largest superfamily among membrane bound proteins that control key physiological functions, such as, neurotransmission, hormone releases, and immune responses among others (Katritch et al., 2013; Lagerström and Schiöth, 2008;Rosenbaum et al., 2009). As such, the large range of integral transmembrane proteins in this family respond to subsequent, diverse array of ligands: including neurotransmitters, hormones, lipids, and odorants (Civelli et al., 2013;Shoichet and Kobilka, 2012). GPCRs in mammals are classified into the five main families according to the GRAFS classification: glutamate, rhodopsin, adhesion, frizzled and secretin (Fredriksson et al., 2003). These five GPCR families are associated with various physiological functions, but the roles of the glutamate and the rhodopsin families are particularly well documented for REVIEW Department of Neuroscience, Functional Pharmacology, Uppsala University, BMC, Box 593,751 24, Uppsala, Sweden.*Authors for correspondence (arunkumar.krishnan@neuro.uu.se; helgi.schioth@neuro.uu.se) neurotransmission and regulation of the nervous system (Niswender and Conn, 2010;Schoepp, 2001). Some functions include synaptic transmission, synapse formation, axon guidance and development of neuronal circuits (Collingridge et al., 2004;Hnasko and Edwards, 2012)...

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Section: N V E C T E N S I S T a D H A E R E N S A Q U E E N S mentioning

confidence: 99%

The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system

Krishnan

Schiöth

2015

Journal of Experimental Biology

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“…The Cys-Hym-33H peptide, or Cys-Hym-33H conjugated to KLH, was used as the immobilized antigen in competitive ELISA (Takahashi et al 2003). Both coating plates gave similar results.…”

Section: Antibody Production and Determination Of Its Specificitymentioning

confidence: 99%

Further characterization of the PW peptide family that inhibits neuron differentiation in Hydra

et al. 2009

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From an evolutionary point of view, Hydra has one of the most primitive nervous systems among metazoans. Two different groups of peptides that affect neuron differentiation were identified in a systematic screening of peptide signaling molecules in Hydra. Within the first group of peptides, a neuropeptide, Hym-355, was previously shown to positively regulate neuron differentiation. The second group of peptides encompasses the PW family of peptides that negatively regulate neuron differentiation. In this study, we identified the gene encoding PW peptide preprohormone. Moreover, we made the antibody that specifically recognizes LPW. In situ hybridization and immunohistochemical analyses showed that the PW peptides and the gene encoding them were expressed in ectodermal epithelial cells throughout the body except for the basal disk. The PW peptides are produced by epithelial cells and are therefore termed "epitheliopeptides." Together with Hym-355, the PW family peptides mediate communication between neurons and epithelial cells and thereby maintain a specific density of neurons in Hydra.

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“…To investigate the possibility that GLW-amide-like peptides exist in the rat brain, we immunostained rat brain tissues with anti-GLW-amide antiserum, which had been raised against the synthetic peptide CGLW-NH 2 conjugated to hemocyanin (Takahashi et al 2003). We detected GLWamide-LI in several regions of the rat central nervous system, including spinal cord.…”

Section: Resultsmentioning

confidence: 99%

“…Then, the sections were incubated with rabbit anti-GLW-amide antisera (Takahashi et al 2003) diluted 1:4000 in PBST-NGS at 4˚C overnight. After several rinses with PBST, the sections were incubated with biotinylated goat anti-rabbit IgG (Vector, Calif., USA) diluted 1:400 in PBST-NGS for 1 h at room temperature, rinsed with PBS several times, incubated with avidin-biotin complex reagent (PK-6100, Vector) for 1 h, and rinsed with PBS for 40 min.…”

Section: Immunohistochemistrymentioning

confidence: 99%

“…The first identified member of this GLW-amide family was metamorphosin A, a peptide that regulates metamorphosis of the lower metazoan, the cnidarian, Hydractinia echinata (Leitz et al 1994). GLW-amide peptides are expressed in neurons and probably function as neuropeptides in cnidaria and Hydra (Gajewski et al 1996;Leitz and Lay 1995;Takahashi et al 2003).…”

Section: Introductionmentioning

confidence: 99%

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Immunohistochemical evidence for the existence of novel mammalian neuropeptides related to the Hydra GLW-amide neuropeptide family

et al. 2009

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The GLW-amide family is a neuropeptide family found in cnidarian species and is characterized by the C-terminal amino acid sequence -Gly-Leu-Trp-NH(2). To detect mammalian peptides structurally related to the GLW-amide family, we examined rat brain by immunohistochemistry with an anti-GLW-amide antibody. GLW-amide-like immunoreactivity (GLW-amide-LI) was observed in thin varicose fibers in some regions of the brain. Most neurons showing GLW-amide-LI were observed in the laterodorsal tegmental nucleus, pedunculopontine tegmental nucleus, and trigeminal/spinal ganglia. These results strongly suggest that the rat nervous system contains as yet unidentified GLW-amide-like peptides, and that GLW-amide-LI in the brain is a good marker for ascending projections from mesopontine cholinergic neurons.

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Identification of a new member of the GLWamide peptide family: physiological activity and cellular localization in cnidarian polyps

Cited by 50 publications

References 30 publications

The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system

The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system

Further characterization of the PW peptide family that inhibits neuron differentiation in Hydra

Immunohistochemical evidence for the existence of novel mammalian neuropeptides related to the Hydra GLW-amide neuropeptide family

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