Abstract
Spexin (Spx), an endogenous peptide, is considered to be a neuropeptide. In a few fish and mammals, it has been proved to play a role in the regulation of animal feeding. However, the possible mechanisms of spexin regulating food intake are mostly blurry in vertebrates including Siberian sturgeon. In this study, firstly, the coding sequence of spexin cDNA was cloned and sequenced in Siberian sturgeon. Then, we detected that spexin mRNA was widely expressed in the hypothalamus, gastrointestinal tract, and liver, with the highest expression in the hypothalamus. The expression of spexin mRNA in the hypothalamus was significantly increased after food intake. At 1 h, 3 h, and 6 h after injection, the food intake in the spexin group (0.10, 0.30, and 0.90 μg/g BW) was significantly lower than that in the saline group. Moreover, compared with the saline group, the mRNA expression of anorectic nucb2, cart, ucn3, and pyy in the hypothalamus was significantly upregulated and orectic npy was significantly downregulated at 1 h after spexin injection; in the stomach, the mRNA expression of nucb2 and pyy was significantly upregulated. All in all, these results provide evidence for the anorexic effect of spexin on Siberian sturgeon.
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Abbreviations
- nucb2:
-
Nucleobindin-2
- cart:
-
Cocaine-and amphetamine-regulated transcript
- ucn3:
-
Urocortin 3
- pyy:
-
Peptide yy
- cck:
-
Cholecystokinin
- npy:
-
Neuropeptide y
- qPCR:
-
Real-time fluorescence quantification PCR
- ORF:
-
Open reading frame
References
CL A, JL J, TF Ø (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64(15):5245. https://doi.org/10.1158/0008-5472.CAN-04-0496
Deng S, Chen H, Zhai Y, Jia L, Liu J, Wang M, Jiang D, Wu T et al (2018) Molecular cloning, characterization and expression analysis of spexin in spotted scat (Scatophagus argus). Gen Comp Endocrinol:S0016648018301588. https://doi.org/10.1016/j.ygcen.2018.04.018
Gibson CD, Carnell S, Ochner CN, Geliebter A (2010) Neuroimaging, gut peptides and obesity: novel studies of the neurobiology of appetite. J Neuroendocrinol 22:833–845. https://doi.org/10.1111/j.1365-2826.2010.02025.x
Hongwei W, Fangjun L, Hu C, Ju L, Yundi G, Xin Z, Jin H, Defang C et al (2016) Ya-fish (Schizothorax prenanti) spexin: identification, tissue distribution and mRNA expression responses to periprandial and fasting. Fish Physiol Biochem 42:39–49. https://doi.org/10.1007/s10695-015-0115-0
Izard JW, Doughty MB, Kendall DAJB (1995) Physical and conformational properties of synthetic idealized signal sequences parallel their biological function. Biochemistry 34:9904–9912. https://doi.org/10.1021/bi00031a012
Jain S, Singh SN (2018) Regulation of food intake: a complex process. Def Life Sci J 3:182–189. https://doi.org/10.14429/dlsj.3.12401
Janssen P, Berghe PV, Verschueren S, Lehmann A, Depoortere I, Tack J (2011) Review article: the role of gastric motility in the control of food intake. Aliment Pharmacol Ther 33:880–894. https://doi.org/10.1111/j.1365-2036.2011.04609.x
Kim D-K, Yun S, Son GH, Hwang J-I, Park CR, Kim JI, Kim K, Vaudry H et al (2014) Coevolution of the spexin/galanin/kisspeptin family: spexin activates galanin receptor type II and III. Endocrinology 155:1864–1873. https://doi.org/10.1210/en.2013-2106
Kolodziejski PA, Pruszynska-Oszmalek E, Micker M, Skrzypski M, Wojciechowicz T, Szwarckopf P, Skieresz-Szewczyk K, Nowak KW et al (2018) Spexin: a novel regulator of adipogenesis and fat tissue metabolism. Biochim Et Biophys Acta Mol Cell Biol Lipids 1863:1228–1236. https://doi.org/10.1016/j.bbalip.2018.08.001
Kołodziejskii P, PruszyńskaOszmałek E, Korek E, Sassek M, Szczepankiewicz D, Kaczmarek P, Nogowski L, Maćkowiak P et al (2017) Serum levels of spexin and kisspeptin negatively correlate with obesity and insulin resistance in women. Physiol Res 67:45–56. https://doi.org/10.33549/physiolres.933
Lee MYM, Soga T, Parhar I (2019) Evolution of structural and functional diversity of Spexin in mammalian and non-mammalian vertebrate species. Front Endocrinol 10:379. https://doi.org/10.3389/fendo.2019.00379
Li SC, Goto NK, Williams KA, Deber CM (1996) Alpha-helical, but not beta-sheet, propensity of proline is determined by peptide environment. Proc Natl Acad Sci U S A 93:6676–6681. https://doi.org/10.1073/pnas.93.13.6676
Li S, Liu Q, Xiao L, Chen H, Li G, Zhang Y, Lin H (2016) Molecular cloning and functional characterization of spexin in orange-spotted grouper (Epinephelus coioides). Comp Biochem Physiol B Biochem Mol Biol 196:85–91. https://doi.org/10.1016/j.cbpb.2016.02.009
Lin C-y, Zhang M, Huang T, Yang L-l, Fu H-b, Zhao L, Zhong LLD, Mu H-X et al (2015) Spexin enhances bowel movement through activating L-type voltage-dependent calcium channel via galanin receptor 2 in mice. Sci Rep 5. https://doi.org/10.1038/srep12095
Lin C-y, Zhao L, Huang T, Lu L, Khan M, Liu J, Zhong LLD, Cai Z-w et al (2018) Spexin acts as novel regulator for bile acid synthesis. Front Physiol 9. https://doi.org/10.3389/fphys.2018.00378
Liping GU, Mingyu GU, Zhang Y, Yan S, Na LI, Yuhang MA, Ding X, Wang Y et al (2016) Correlation between serum Spexin level and blood glucose and lipids in patients with type 2 diabetes. Shanghai Med J 15:345–351
Ma A, He M, Bai J, Wong MKH, Ko WKW, Wong AOL (2017) Dual role of insulin in spexin regulation: functional link between food intake and spexin expression in a fish model. Endocrinology 158:560–577. https://doi.org/10.1210/en.2016-1534
Martin F, Frank K, Norton T, Svendsen E, Alfredsen JA, Dempster T, Eguiraun H, Watson W et al (2017) Precision fish farming: a new framework to improve production in aquaculture. Biosyst Eng:S1537511017304488. https://doi.org/10.1016/j.biosystemseng.2017.10.014
Mirabeau O, Perlas E, Severini C, Audero E, Gascuel O, Possenti R, Birney E, Rosenthal N et al (2007) Identification of novel peptide hormones in the human proteome by hidden Markov model screening. Genome Res 17:320–327. https://doi.org/10.1101/g.5755407
Porzionato A, Rucinski M, Macchi V, Stecco C, Malendowicz LK, De Caro R (2010) Spexin Expression in normal rat tissues. J Histochem Cytochem 58:825–837. https://doi.org/10.1369/jhc.2010.956300
Rønnestad I, Gomes AS, Murashita K, Angotzi R, Jönsson E, Volkoff H (2017) Appetite-controlling endocrine systems in teleosts. Front Endocrinol 8:73. https://doi.org/10.3389/fendo.2017.00073
Sassek M, Kolodziejski PA, Strowski MZ, Nogowski L, Nowak KW, Mackowiak P (2018a) Spexin modulates functions of rat endocrine pancreatic cells. Pancreas 47:904–909. https://doi.org/10.1097/mpa.0000000000001083
Sassek M, Kolodziejski PA, Szczepankiewicz D, Pruszynska-Oszmalek E (2018b) Spexin in the physiology of pancreatic islets-mutual interactions with insulin. Endocrine. https://doi.org/10.1007/s12020-018-1766-2
Sonmez K, Zaveri NT, Kerman IA, Burke S, Neal CR, Xie X, Watson SJ, Toll L (2009) Evolutionary sequence modeling for discovery of peptide hormones. PLoS Comput Biol 5:e1000258. https://doi.org/10.1371/journal.pcbi.1000258
Walewski JL, Ge F, Lobdell H, Levin N, Schwartz GJ, Vasselli JR, Pomp A, Dakin G et al (2014) Spexin is a novel human peptide that reduces adipocyte uptake of long chain fatty acids and causes weight loss in rodents with diet-induced obesity. Obesity 22:1643–1652. https://doi.org/10.1002/oby.20725
Wang S, Wang B, Chen S (2018) Spexin in the half-smooth tongue sole (Cynoglossus semilaevis): molecular cloning, expression profiles, and physiological effects. Fish Physiol Biochem:1–11. https://doi.org/10.1007/s10695-018-0472-6
Williot P, Nonnotte G, Chebanov M (2009) Siberian sturgeon (Acipenser Baeri, Brandt JF 1869) gut: anatomic description. Int Aquat Res 1:45–60
Wong MK, Sze KH, Chen T, Cho CK, Law HC, Chu IK, Wong AO (2013) Goldfish spexin: solution structure and novel function as a satiety factor in feeding control. Am J Physiol Endocrinol Metab 305:E348–E366. https://doi.org/10.1152/ajpendo.00141.2013
Wu H, Lin F, Chen H, Liu J, Gao Y, Zhang X, Hao J, Chen D et al (2016) Ya-fish (Schizothorax prenanti) spexin: identification, tissue distribution and mRNA expression responses to periprandial and fasting. Fish Physiol Biochem 42:39–49. https://doi.org/10.1007/s10695-015-0115-0
Yáñez J, Anadón R (1998) Neural connections of the pineal organ in the primitive bony fish Acipenser baeri: a carbocyanine dye tract-tracing study. J Comp Neurol 398:151–161. https://doi.org/10.1002/(sici)1096-9861(19980824)398:2 < 151::aid-cne1>3.0.co;2-#
Yun RH, Anderson A, Hermans DJ (1991) Proline in α-helix: Stability and conformation studied by dynamics simulation. Proteins 10:219–228. https://doi.org/10.1002/prot.340100306
Zhang X, Tang N, Qi J, Wang S, Hao J, Wu Y, Chen H, Tian Z et al (2017) CCK reduces the food intake mainly through CCK1R in Siberian sturgeon (Acipenser baerii Brandt). Sci Rep 7:12413. https://doi.org/10.1038/s41598-017-12,646-3
Zhang X, Qi J, Tang N, Wang S, Wu Y (2018a) Intraperitoneal injection of nesfatin-1 primarily through the CCK-CCK1R signal pathway affects expression of appetite factors to inhibit the food intake of Siberian sturgeon (Acipenser baerii). Peptides 109:14–22. https://doi.org/10.1016/j.peptides.2018.09.008
Zhang X, Wang S, Chen H, Tang N, Qi J, Wu Y, Hao J, Tian Z et al (2018b) The inhibitory effect of NUCB2/nesfatin-1 on appetite regulation of Siberian sturgeon (Acipenser baerii Brandt). Horm Behav 103:111–120. 103:111–120. https://doi.org/10.1016/j.yhbeh.2018.06.008
Zheng B, Li S, Liu Y, Li Y, Chen H, Tang H, Liu X, Lin H et al (2017) Spexin suppress food intake in zebrafish: evidence from gene knockout study. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-15,138-6A
Acknowledgments
We are very thankful to the company of Runzhao Fisheries (Sichuan, China) for supplying fish and Sichuan Agricultural University for available experimental platform.
Funding
This study was financially supported by the Sichuan Science and Technology Program (2019YJ0438).
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This study was complied with the ethical statements. All experiments were approved by the Animal Care and Use Committee of Sichuan Agricultural University and followed the guidelines for animal experiments of Sichuan Agricultural University (No. DKY-S20150812).
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Highlights
• The partial cDNA sequence and tissue distribution of Siberian sturgeon spexin gene were shown.
• The mRNA expression of spexin increased after feeding in Siberian sturgeon hypothalamus.
• Intraperitoneal injection with spexin reduced the food intake of Siberian sturgeon and changed the mRNA expression of some appetite-regulating factors in both hypothalamus and stomach.
Zhengzhi Tian, Shaoqi Xu, Mei Wang, and Ya Li paid a similar amount of work and carried out experiments and thesis writing. Zhengzhi Tian, Shaoqi Xu, Mei Wang, Ya Li, Ni Tang, and Bin Wang participated in animal experiments. All authors participated in experimental design and thesis writing.
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Tian, Z., Xu, S., Wang, M. et al. Identification, tissue distribution, periprandial expression, and anorexigenic effect of spexin in Siberian sturgeon, Acipenser baeri. Fish Physiol Biochem 46, 2073–2084 (2020). https://doi.org/10.1007/s10695-020-00856-y
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DOI: https://doi.org/10.1007/s10695-020-00856-y