Introduction
Peptides related to vertebrate tachykinins were first identified from the locust Locusta migratoria using a hindgut contraction assay for isolation (Schoofs et al., 1990). These peptides were designated locustatachykinins (LomTKs). Further TKs from other insects and crustaceans were isolated and it was found that they possess a conserved C-terminus FX1GX2Ramide (X1 and X2 are variable residues) and range between 7 and 19 amino acids (see Nässel 1999; Van Loy et al., 2010). The first gene encoding a TK precursor was identified in Drosophila (Siviter et al., 2000). From this precursor six TKs (DTK1-6) can be cleaved, one of which is extended and has a G to A substitution in the C-terminus: FVAVRa. Cockroach precursors contain 13 copies of TKs (LemTRP1-13 and PeaTRP1-13) two of which are N-terminally extended and predominantly expressed in the intestine (Predel et al., 2005). Originally two receptors were proposed as tachykinin receptors in Drosophila, DTKR (Takr99D; CG7887) and NKD (Takr86C; CG6515) (Li et al., 1991; Monnier et al., 1992). One of these (Takr99D; CG7887) was confirmed as a receptor for DTK1-5 (Birse et al., 2006), whereas the NKD was identified as the receptor of natalisins, peptides remotely related to tachykinins (Jiang et al., 2013). It can be noted that in salivary glands of cephalopods and the mosquito Aedes aegypti peptides were identified that are more similar to vertebrate tachykinins; these are referred to an invertebrate tachykinins (InvTKs) (Kanda et al., 2003; Satake et al., 2003). The mosquito sequence is SGNTGDKFYGLMa and that of mammalian substance P is RPKPQQFFGLMa.
Location
TRPs are widely distributed in numerous interneurons of the CNS, sets of brain neurosecretory cells, as well as enteroendocrine cells of the midgut in many insect species studied (Muren et al., 1995; Siviter et al., 2000; Winther and Nässel, 2001; Kwok et al 2005; Kahsai et al., 2010). The interneurons expressing TRPs innervate a wide range of brain neuropils, including central complex, antennal lobes, optic lobes, and in some species the mushroom bodies.
Function
The original studies indicated roles of TRPs in modulation of contractions of various visceral muscles in different insects and a regulation of release of adipokinetic hormone from the corpora cardiaca in locusts (see Nässel, 1999; Van Loy et al., 2010). More recently, wide range of functions has been revealed for TRPs, especially in Drosophila. These include modulation of olfactory inputs in the antennal lobe (Ignell et al., 2009; Ko et al., 2015), central modulation of walking behaviour (Kahsai et al., 2010), modulation of stress responses (Kahsai et al., 2010), regulation of insulin producing neurons (Birse et al., 2011), control of aggression in male flies (Asahina et al., 2014), regulation of pheromone detection (Shankar et al., 2015), mediation of thermal nociceptive signals (Im et al., 2015), and finally, TRPs from midgut endocrine cells regulate lipid production in the intestine (Song et al., 2014). Thus, the TRPs may be an example of peptides with multiple distributed functions.
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Suggested Reviews
- Nässel, D.R. (1999). Tachykinin-related peptides in invertebrates: a review. Peptides 20(1), 141-158. doi: S0196-9781(98)00142-9 [pii].
View Review
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Satake H, Kawada T, Nomoto K, Minakata H. (2003) Insight into tachykinin-related peptides, their receptors, and invertebrate tachykinins: a review. Zoolog Sci. 20:533-49.
View Review
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Van Loy, T., Vandersmissen, H.P., Poels, J., Van Hiel, M.B., Verlinden, H., and Vanden Broeck, J. (2010). Tachykinin-related peptides and their receptors in invertebrates: a current view. Peptides 31(3), 520-524. doi: 10.1016/j.peptides.2009.09.023.
View Review
References
- Ignell, R., Root, C.M., Birse, R.T., Wang, J.W., Nässel, D.R., and Winther, Å.M. (2009). Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci U S A 106, 13070-13075.
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Im, S.H., Takle, K., Jo, J., Babcock, D.T., Ma, Z., Xiang, Y., and Galko, M.J. (2015). Tachykinin acts upstream of autocrine Hedgehog signalling during nociceptive sensitization in Drosophila. eLife 4, e10735.
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Jiang, H., Lkhagva, A., Daubnerova, I., Chae, H.S., Simo, L., Jung, S.H., Yoon, Y.K., Lee, N.R., Seong, J.Y., Zitnan, D., Park, Y., and Kim, Y.J. (2013). Natalisin, a tachykinin-like signalling system, regulates sexual activity and fecundity in insects. Proceedings of the National Academy of Sciences of the United States of America 110, E3526-3534.
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Kanda, A., Iwakoshi-Ukena, E., Takuwa-Kuroda, K., and Minakata, H. (2003). Isolation and characterization of novel tachykinins from the posterior salivary gland of the common octopus Octopus vulgaris. Peptides 24, 35-43.
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Kahsai, L., Kapan, N., Dircksen, H., Winther, Å.M., and Nässel, D.R. (2010). Metabolic stress responses in Drosophila are modulated by brain neurosecretory cells that produce multiple neuropeptides. PLoS ONE 5, e11480.
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Kahsai, L., Martin, J.R., and Winther, Å.M. (2010). Neuropeptides in the Drosophila central complex in modulation of locomotor behaviour. J Exp Biol 213, 2256-2265.
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Ko, K.I., Root, C.M., Lindsay, S.A., Zaninovich, O.A., Shepherd, A.K., Wasserman, S.A., Kim, S.M., and Wang, J.W. (2015). Starvation promotes concerted modulation of appetitive olfactory behaviour via parallel neuromodulatory circuits. eLife 4.
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Kwok, R., Chung, D., Brugge, V.T., and Orchard, I. (2005). The distribution and activity of tachykinin-related peptides in the blood-feeding bug, Rhodnius prolixus . Peptides 26, 43-51.
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Li XJ, Wolfgang W, Wu YN, North RA, Forte M. 1991. Cloning, heterologous expression and developmental regulation of a Drosophila receptor for tachykinin-like peptides. EMBO J 10(11):3221-3229.
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Monnier D, Colas JF, Rosay P, Hen R, Borrelli E, Maroteaux L. 1992. NKD, a developmentally regulated tachykinin receptor in Drosophila. J Biol Chem 267(2):1298-1302.
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Muren, J.E., Lundquist, C.T., and Nässel, D.R. (1995). Abundant distribution of locustatachykinin-like peptide in the nervous system and intestine of the cockroach Leucophaea maderae. Philos Trans R Soc Lond B Biol Sci 348, 423-444.
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Predel R, Neupert S, Roth S, Derst C, Nässel DR. 2005. Tachykinin-related peptide precursors in two cockroach species. FEBS journal 272(13):3365-3375.
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Satake H, Kawada T, Nomoto K, Minakata H. 2003. Insight into tachykinin-related peptides, their receptors, and invertebrate tachykinins: a review. Zoological science 20(5):533-549.
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Schoofs, L., Holman, G.M., Hayes, T.K., Nachman, R.J., and De Loof, A. (1990). Locustatachykinin I and II, two novel insect neuropeptides with homology to peptides of the vertebrate tachykinin family. FEBS letters 261(2), 397-401.
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Shankar, S., Chua, J.Y., Tan, K.J., Calvert, M.E., Weng, R., Ng, W.C., Mori, K., and Yew, J.Y. (2015). The neuropeptide tachykinin is essential for pheromone detection in a gustatory neural circuit. eLife 4, e06914.
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Siviter RJ, Coast GM, Winther AM, Nachman RJ, Taylor CA, Shirras AD, Coates D, Isaac RE, Nassel DR. 2000. Expression and functional characterization of a Drosophila neuropeptide precursor with homology to mammalian preprotachykinin A. J Biol Chem 275(30):23273-23280.
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Song, W., Veenstra, J.A., and Perrimon, N. (2014). Control of lipid metabolism by tachykinin in Drosophila. Cell reports 9, 40-47.
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Winther, Å.M.E., and Nässel, D.R. (2001). Intestinal peptides as circulating hormones: Release of tachykinin-related peptide from the locust and cockroach midgut. J Exp Biol 204, 1269-1280.