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Review
.2022 Dec 16:13:1056939.
doi: 10.3389/fendo.2022.1056939. eCollection 2022.

Tachykinins, new players in the control of reproduction and food intake: A comparative review in mammals and teleosts

Affiliations
Review

Tachykinins, new players in the control of reproduction and food intake: A comparative review in mammals and teleosts

Aurora Campo et al. Front Endocrinol (Lausanne)..

Abstract

In vertebrates, the tachykinin system includes tachykinin genes, which encode one or two peptides each, and tachykinin receptors. The complexity of this system is reinforced by the massive conservation of gene duplicates after the whole-genome duplication events that occurred in vertebrates and furthermore in teleosts. Added to this, the expression of the tachykinin system is more widespread than first thought, being found beyond the brain and gut. The discovery of the co-expression of neurokinin B, encoded by the tachykinin 3 gene, and kisspeptin/dynorphin in neurons involved in the generation of GnRH pulse, in mammals, put a spotlight on the tachykinin system in vertebrate reproductive physiology. As food intake and reproduction are linked processes, and considering that hypothalamic hormones classically involved in the control of reproduction are reported to regulate also appetite and energy homeostasis, it is of interest to look at the potential involvement of tachykinins in these two major physiological functions. The purpose of this review is thus to provide first a general overview of the tachykinin system in mammals and teleosts, before giving a state of the art on the different levels of action of tachykinins in the control of reproduction and food intake. This work has been conducted with a comparative point of view, highlighting the major similarities and differences of tachykinin systems and actions between mammals and teleosts.

Keywords: endokinin/hemokinin; food intake; mammals; neurokinins; reproduction; substance P; tachykinins; teleosts.

Copyright © 2022 Campo, Dufour and Rousseau.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Comparison of the tachykinin system in a mammal, the human, and in a teleost, the grass carp. In human(A), the tachykinin system comprises threetac genes (tac1,tac2, andtac3) encoding up to 10 different TAC peptides (SP, NKA, NPK, and NPγ for thetac1 gene; HK1, EKA, EKB, EKC, and EKC for thetac4 gene; NKB for thetac3 gene) due to the existence of various spliced variants (α, β, γ, and δ for the tac1 and tac4 genes; (α, β, and γ for the tac3 gene). These human TAC peptides bind to three TACR (TACR1, TAC2, and TACR3) with different affinities: SP, HK1, EKA, and EKB for TACR1; NKA, NPK, and NPγ for TACR2; NKB for TACR3. In teleosts(B), due to the teleost-specific whole-genome duplication (3R), duplicates fortac1 (tac1a andtac1b),tac3 (tac3a andtac3b), andtac4 (tac4a andtac4b) exist and up to 12 different TAC peptides have been identified up to now. Up to six TACR have been yet characterized: two TACR1 (TACR1a and TACR1b), one TACR2, and three TACR3 (TACR3a1, TACR3a2, and TACR3b). One of the 3R-duplicatedtacr2 paralogs (tacr2b) was lost in the teleost lineage but conserved in the eels (elopomorphs) (Campo et al. in preparation). Binding studies with the complete available tachykinin system have only been performed in the grass carp, the unique teleost species for now in which thetac4 gene has been identified and published. In this species,tac4b andtacr2b have not yet been identified and appear in transparency in the figure. For more information, please refer to part 1 of this review. EKA, endokinin A; EKB, endokinin B; EKC, endokinin C; EKD, endokinin D; HK1, hemokinin 1; HK2, hemokinin 2; NKA, neurokinin A; NKB, neurokinin B; NKBRP, neurokinin B-related peptide; NPK, neuropeptide K; NPγ, neuropeptide gamma; SP, substance P; TAC, tachykinin peptide;tac, tachykinin gene; TACR, tachykinin receptor (protein);tacr, tachykinin receptor gene.
Figure 2
Figure 2
Direct effects of TAC peptides in the control of reproductive function in mammals and teleosts. TAC peptides can act directly at all the levels of the HPG axis (hypothalamus, pituitary, gonads in both mammals(A) and teleosts(B), and other peripheral reproductive organs in mammals). At the brain level (hypothalamus), the effect of TAC on GnRH is likely kisspeptin-dependent in both mammals (KNDy neurons) and teleosts. At the pituitary level, while TAC action is only stimulatory on gonadotropins in mammals, a species specificity is observed in teleosts with either no, stimulatory, or inhibitory effects. At the peripheral level, TAC can act on ovarian steroidogenesis in mammals (either no, positive, or negative effects) and teleosts (positive effects). In mammals, a positive effect is also noted on the contraction of secondary sex organs (uterus in females; vas deferens, seminal vesicles, and prostate gland in male), as well as on sperm motility in males. For more details and for data fromin vivo experiments, please refer to part 2 of this review and toTable 1. +, direct stimulatory effect; -, direct inhibitory effect; 0, no direct effect; cyp11a1, gene encoding cholesterol side-chain cleavage enzyme P450scc; cyp19a1, gene encoding aromatase; Dyn, dynorphin; E2, estradiol; ESR, nuclear estrogen receptor; FSH, follicle-stimulating hormone; GnRH, gonadotropin-releasing hormone; GnIH-R, gonadotropin-inhibitory hormone receptor; GPER, G-protein-coupled (membrane) estrogen receptor; hCG, human chorionic gonadotropin; HK1, hemokinin 1; HK2, hemokinin 2; kiss, kisspeptin; LH, luteinizing hormone; NKA, neurokinin A; NKB, neurokinin B; NPK, neuropeptide K; NPγ, neuropeptide gamma; P, progesterone; SP, substance P; T, testosterone.
Figure 3
Figure 3
Direct effects of TAC peptides in the control of food intake and gut motility in mammals and teleosts. TAC peptides can act directly at different levels (hypothalamus, pituitary, and gastrointestinal tract) to influence food intake and gut motility. In mammals(A), most of the available studies report the stimulatory effects of tachykinins on gut motility. In teleosts(B), recentin vitro studies are emerging, showing direct effects of TAC3 and TAC4 peptides on the expression of neuropeptides highly expressed in the pituitary and that are involved in the central control of food intake. These TAC peptides can also influence the expression of genes from the gut that control its motility. For more details and for data fromin vivo experiments, please refer to part 3 of this review. +, direct stimulatory effect; -, direct inhibitory effect; 0, no direct effect; AgRP, agouti related peptide; CART, cocaine and amphetamine regulated transcript; CCK, cholescystokinin; HK2, hemokinin 2; NKA, neurokinin A; NKB, neurokinin B; NMB, neuromedin B; NPY, neuropeptide Y; POMC, proopiomelanocortin; PYY, peptide YY; SP, substance P.
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