The evolution of tachykinin/tachykinin receptor (TAC/TACR) in vertebrates and molecular identification of the TAC3/TACR3 system in zebrafish (Danio rerio)

Zhou, Wei; Li, Shuisheng; Liu, Yun; Qi, Xin; Chen, Huapu; Chen, Cheng; Liu, Xiaochun; Zhang, Yong; Lin, Haoran

doi:10.1016/j.mce.2012.04.007

Cited by 44 publications

(66 citation statements)

References 55 publications

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“…In vertebrates tachykinin and the TRPs form a group of ancestral neuropeptides that are found in a wide range of animals, from octopus to human (14)(15)(16)(17)(18). In insects, multiple paracopies of the TRP gene contain the C-terminal FxGxRamide motif, whereas vertebrate tachykinins typically contain the FxGLMamide motif (Fig.…”

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confidence: 99%

Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects

Jiang

Lkhagva

Daubnerová

et al. 2013

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

120

166

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An arthropod-specific peptidergic system, the neuropeptide designated here as natalisin and its receptor, was identified and investigated in three holometabolous insect species: Drosophila melanogaster, Tribolium castaneum, and Bombyx mori. In all three species, natalisin expression was observed in 3-4 pairs of the brain neurons: the anterior dorso-lateral interneurons, inferior contralateral interneurons, and small pars intercerebralis neurons. In B. mori, natalisin also was expressed in two additional pairs of contralateral interneurons in the subesophageal ganglion. Natalisin-RNAi and the activation or silencing of the neural activities in the natalisin-specific cells in D. melanogaster induced significant defects in the mating behaviors of both males and females. Knockdown of natalisin expression in T. castaneum resulted in significant reduction in the fecundity. The similarity of the natalisin C-terminal motifs to those of vertebrate tachykinins and of tachykinin-related peptides in arthropods led us to identify the natalisin receptor. A G protein-coupled receptor, previously known as tachykinin receptor 86C (also known as the neurokinin K receptor of D. melanogaster), now has been recognized as a bona fide natalisin receptor. Taken together, the taxonomic distribution pattern of the natalisin gene and the phylogeny of the receptor suggest that natalisin is an ancestral sibling of tachykinin that evolved only in the arthropod lineage.N europeptides are ancestral signaling molecules that function as cell-cell communication mediators in multicellular organisms. Large numbers of diverse neuropeptides are involved in the control of animal behavior, development, and physiology. Recent genomic approaches have revealed diverse groups of neuropeptides in different taxa, based on similarities in the amino acid sequences to neuropeptides discovered in earlier physiological and anatomical studies (1-4). Sequenced genomes of many insect species (5) provide an opportunity to explore the evolutionary processes of neuropeptides and their receptors. Furthermore, the tools available in biotechnology that are readily applicable in suitable insect model species have advanced our understanding of the functions of neuropeptides. Drosophila melanogaster has been the best model system, allowing functional studies of neuropeptides and their receptors by the use of highly advanced molecular genetic tools and various publicly available resources (6). A number of other insect species, especially those with sequenced genomes, such as Bombyx mori and Tribolium castaneum, also have been used for investigations into the functions of neuropeptide signals, using piggyBac transformation (7) and RNAi (8,9).Previous studies on insect neuropeptides and their G proteincoupled receptors (GPCRs) have described tachykinin-related peptides (TRPs) and two GPCRs as the receptors for the TRPs in D. melanogaster and other insect species (10-14). In vertebrates tachykinin and the TRPs form a group of ancestral neuropeptides that are found in a wide rang...

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confidence: 99%

Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects

Jiang

Lkhagva

Daubnerová

et al. 2013

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

120

166

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“…3B). The zebrafish Tacr2 (predicted sequence) and Tacr3 (Zhou et al 2012) amino acid sequences were used to check whether Tacr1a and Tacr1b could be aligned in Tacr2 or Tacr3 clusters and might not be duplicate genes. The phylogenetic analyses showed that Tacr1a and Tacr1b were aligned in the same cluster of Tacr1s, suggesting that Tacr1a and Tacr1b receptors are duplicate genes and paralogs of the Tacr2 and Tacr3 from zebrafish and orthologs of the TACR1, TACR2, and TACR3 of several species.…”

Section: Phylogenetic Analysis Of Zebrafish Tacr1a and Tacr1bmentioning

confidence: 99%

“…The following species (with their respective accession number) were employed to perform the phylogenetic analyses in the case of TAC1R: human (NP_001049.1), dog (NP_001012637.1), guinea pig (NP_001166332.1), rat (NP_036799.1), mouse (NP_033339.2), chicken (NP_990199.1), frog (NP_001106489.1; Xenopus tropicalis), fugu (AAQ02694), zebrafish Tacr1a (GenBank ID: 33455), and zebrafish Tacr1b (GenBank ID: 345672; also named Nk1a and Nk1b respectively); for TACR2: human (NP_001048.2), rat (NP_542946.1), mouse (NP_033340.2), and zebrafish Tacr2 (XP_001341981.1) (predicted sequence); in the case of TACR3: human (NP_001050.1), rat (NP_058749.1), mouse (NP_067357.1), and zebrafish Tacr3a1, Tacr3a2, and Tacr3b (Zhou et al 2012).…”

Section: Phylogenetic Analysis Of Zebrafish Tacr1a and Tacr1bmentioning

confidence: 99%

“…The biological actions of the tachykinin family -substance P (SP), neurokinin A (NKA) and NKB, hemokinin-1, and endokinins -are mediated by transmembrane G-proteincoupled receptors (GPCRs) and they have been classified within the NK 1 , NK 2 , and NK 3 receptor types (Regoli et al 1994, Maggi 2000, Harrison & Geppetti 2001, Pennefather et al 2004, which are encoded by tachykinin receptor 1 (TACR1), TACR2, and TACR3 genes respectively (Zhou et al 2012). SP, NKA, and NKB bind to NK 1 , NK 2 , and NK 3 receptors (also named TACR1, TACR2, and TACR3) respectively (Regoli et al 1987, Regoli et al 1994, DeVane 2001, Harrison & Geppetti 2001.…”

Section: Introductionmentioning

confidence: 99%

“…Recently, the tac1, tac2, and tac3 precursors and the Tacr3s (Tacr3a1, Tacr3a2, and Tacr3b; Ogawa et al 2012, Zhou et al 2012) have been cloned. Taking the above into consideration, we aimed to i) clone the tacr1 gene and study its expression during embryogenesis, ii) determine the evolutionary history of the tacr1s using phylogenetic analyses, iii) investigate the effects of cocaine on the tacr1s, and iv) study the interrelationship between the tachykinin system and opioid receptors during embryonic development.…”

Section: Introductionmentioning

confidence: 99%

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Expression of tachykinin receptors (tacr1a and tacr1b) in zebrafish: influence of cocaine and opioid receptors

López-Bellido¹,

Barreto-Valer²,

Rodrı́guez³

2012

Journal of Molecular Endocrinology

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Opioid and tachykinin receptors (TACRs) are closely related in addiction and pain processes. In zebrafish, opioid receptors have been cloned and characterized both biochemically and pharmacologically. However, the tacr1 gene has not yet been described in zebrafish. The aim of this research was to identify the tacr1 gene, study the effects of cocaine on tacr1, and analyze the interaction between tacr1 and opioid receptors. We have identified a duplicate of tacr1 gene in zebrafish, designated as tacr1a and tacr1b. Phylogenetic analyses revealed an alignment of these receptors in the Tacr1 fish cluster, with a clear distinction from other TACR1s of amphibians, birds, and mammals. Our qPCR results showed that tacr1a and tacr1b mRNAs are expressed during embryonic development. Whole-mount in situ hybridization showed tacr1 expression in the CNS and in the peripheral tissues. Cocaine (1.5 mM) induced an upregulation of tacr1a and tacr1b at 24 and 48 h post-fertilization (hpf; except for tacr1a at 48 hpf, which was downregulated). By contrast, HEK-293 cells transfected with tacr1a and tacr1b and exposed to cocaine showed a downregulation of tacr1s. The knockdown of ZfDOR2 and ZfMOR, opioid receptors, induced a down-and upregulation of tacr1a and tacr1b respectively. In conclusion, tacr1a and tacr1b in zebrafish are widely expressed throughout the CNS and peripherally, suggesting a critical role of these tacr1s during embryogenesis. tacr1a and tacr1b mRNA expression is altered by cocaine exposure and by the knockdown of opioid receptors. Thus, zebrafish can provide clues for a better understanding of the relationship between tachykinin and opioid receptors in pain and addiction during embryonic development.

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Expression of tachykinin3 and related reproductive markers in the brain of the African cichlid fish Astatotilapia burtoni

Butler

Maruska

2019

J of Comparative Neurology

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Neurokinin B, encoded by the tachykinin3 gene, plays a crucial role in regulating reproduction in mammals via KNDy neurons and interaction with GnRH. Previous work in teleost fishes has focused on hypothalamic tac3 expression for its role in reproduction, but detailed studies on extra‐hypothalamic tac3 expression are limited. Here, we identified two tac3 genes in the social African cichlid fish Astatotilapia burtoni, only one of which produces a functional protein containing the signature tachykinin motif. In situ hybridization for tac3a mRNA identified cell populations throughout the brain. Numerous tac3a cells lie in several thalamic and hypothalamic nuclei, including periventricular nucleus of posterior tuberculum, lateral tuberal nucleus (NLT), and nucleus of the lateral recess (NRL). Scattered tac3‐expressing cells are also present in telencephalic parts, such as ventral (Vv) and supracomissural (Vs) part of ventral telencephalon. In contrast to other teleosts, tac3 expression was absent from the pituitary. Using double‐fluorescent staining, we localized tac3a‐expressing cells in relation to GnRH and kisspeptin cells. Although no GnRH‐tac3a colabeled cells were observed, dense GnRH fibers surround and potentially synapse with tac3a cells in the preoptic area. Only minimal (<5%) colabeling of tac3a was observed in kiss2 cells. Despite tac3a expression in many nodes of the mesolimbic reward system, it was absent from tyrosine hydroxylase (TH)‐expressing cells, but tac3a cells were located in areas with dense TH fibers. The presence of tac3a‐expressing cells throughout the brain, including in socially relevant brain regions, suggest more diverse functions beyond regulation of reproductive physiology that may be conserved across vertebrates.

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The evolution of tachykinin/tachykinin receptor (TAC/TACR) in vertebrates and molecular identification of the TAC3/TACR3 system in zebrafish (Danio rerio)

Cited by 44 publications

References 55 publications

Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects

Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects

Expression of tachykinin receptors (tacr1a and tacr1b) in zebrafish: influence of cocaine and opioid receptors

Expression of tachykinin3 and related reproductive markers in the brain of the African cichlid fish Astatotilapia burtoni

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