Skip to main content
SpringerLink
Log in

Effects of feeding status on nucb1 and nucb2A mRNA expression in the hypothalamus of Schizothorax davidi

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

NUCB1 and NUCB2, two novel nucleobindins, have attracted extensive attention for their role in the appetite regulation in mammals. However, little is known about the appetite regulation of NUCB1 and NUCB2 in fish species. Therefore, we investigated the role of these peptides in the regulation of feeding in Schizothorax davidi (S. davidi). In this study, full-length cDNA sequences of nucb1 and nucb2A of S. davidi were obtained for the first time. Additionally, the tissue distribution and the effects of different energy status on nucb1 and nucb2A mRNAs abundance were assessed, showing that nucb1 and nucb2A are widely distributed in 18 detected tissues, with the highest expression in the cerebellum. The abundances of nucb1 and nucb2A increased in the hypothalamus at 1 h and 3 h post-feeding. Furthermore, fasting and re-feeding experiments showed that the expressions of nucb1 and nucb2A in hypothalamus significantly decreased after fasting for 7 days, and returned to the control level after re-feeding for 3 or 5 days. In conclusion, the present study suggests that both NUCB1 and NUCB2A are involved in the short-term and long-term appetite regulation, as an anorexigenic factor, in S. davidi. These results can provide a basis for further investigation into the appetite regulatory role of NUCB family in teleost.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Atsuchi K, Asakawa A, Ushikai M, Ataka K, Tsai M, Koyama K, Sato Y, Kato I, Fujimiya M, Inui A (2010) Centrally administered nesfatin-1 inhibits feeding behaviour and gastroduodenal motility in mice. Neuroreport 21:1008–1011

    CAS  PubMed  Google Scholar 

  • Bayes A, Collins MO, Reigviader R, Gou G, Goulding D, Izquierdo A, Choudhary JS, Emes RD, Grant SGN (2017) Evolution of complexity in the zebrafish synapse proteome. Nat Commun 8:14613

    Article  Google Scholar 

  • Bernier NJ, Peter RE (2001) The hypothalamic-pituitary-interrenal axis and the control of food intake in teleost fish. Comp Biochem Physiol B 129:639–644

    Article  CAS  Google Scholar 

  • Chen H, Zhang X, Hao J, Chen D, Liu J, Gao Y, Zhu J, Wu H, Lin F, Pu Y (2015) Molecular cloning, expression analysis, and appetite regulatory effect of peptide YY in Siberian sturgeon (Acipenser baerii). Gene 563:172–179

    Article  CAS  Google Scholar 

  • Coll AP, Farooqi IS, Orahilly S (2007) The hormonal control of food intake. Cell 129:251–262

    Article  CAS  Google Scholar 

  • Gawli K, Ramesh N, Unniappan S (2017) Nesfatin-1-like peptide is a novel metabolic factor that suppresses feeding, and regulates whole-body energy homeostasis in male Wistar rats. PLoS One 12:e0178329

    Article  Google Scholar 

  • Gibbs J, Young RC, Smith GP (1997) Cholecystokinin decreases feed intake in rats. Obes Res 5:284–290

    Article  CAS  Google Scholar 

  • Gonzalez R, Kerbel B, Chun A, Unniappan S (2010) Molecular, cellular and physiological evidences for the anorexigenic actions of nesfatin-1 in goldfish. PLoS One 5

  • Gonzalez R, Mohan H, Unniappan S (2012) Nucleobindins: bioactive precursor proteins encoding putative endocrine factors? Gen Comp Endocrinol 176:341

    Article  CAS  Google Scholar 

  • Hao J, Liu Q, Zhang X, Wu Y, Zhu J, Qi J, Tang N, Wang S, Wang H, Chen D (2017) The evidence of apelin has the bidirectional effects on feeding regulation in Siberian sturgeon (Acipenser baerii). Peptides

  • Hatef A, Shajan S, Unniappan S (2015) Nutrient status modulates the expression of nesfatin-1 encoding nucleobindin 2A and 2B mRNAs in zebrafish gut, liver and brain. Gen Comp Endocrinol 215:51–60

    Article  CAS  Google Scholar 

  • Hayes J, Volkoff H (2014) Characterization of the endocrine, digestive and morphological adjustments of the intestine in response to food deprivation and torpor in cunner, Tautogolabrus adspersus. Comp Biochem Physiol A Mol Integr Physiol 170:46–59

    Article  CAS  Google Scholar 

  • Kerbel B, Unniappan S (2012) Nesfatin-1 suppresses energy intake, co-localises ghrelin in the brain and gut, and alters ghrelin, cholecystokinin and orexin mRNA expression in goldfish. J Neuroendocrinol 24:366–377

    Article  CAS  Google Scholar 

  • Kim J, Chung Y, Kim H, Im E, Lee H, Yang H (2014) The tissue distribution of nesfatin-1/NUCB2 in mouse. Dev Reprod 18:301

    Article  Google Scholar 

  • Lenard NR, Berthoud H (2008) Central and peripheral regulation of food intake and physical activity: pathways and genes. Obesity 16

  • Leong JS, Jantzen SG, Von Schalburg KR, Cooper GA, Messmer AM, Liao NY, Munro S, Moore RA, Holt RA, Jones SJM (2010) Salmo salar and Esox lucius full-length cDNA sequences reveal changes in evolutionary pressures on a post-tetraploidization genome. BMC Genomics 11:279–279

    Article  Google Scholar 

  • Lin F, Zhou C, Chen H, Wu H, Xin Z, Liu J, Gao Y, Yuan D, Wang T, Wei R (2014) Molecular characterization, tissue distribution and feeding related changes of NUCB2A/nesfatin-1 in Ya-fish (Schizothorax prenanti). Gene 536:238–246

    Article  CAS  Google Scholar 

  • Meyer A, De Peer YV (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945

    Article  CAS  Google Scholar 

  • Ohi S, Shimizu H, Satoh T, Okada S, Adachi S, Inoue K, Eguchi H, Yamamoto M, Imaki T, Hashimoto K (2006) Identification of nesfatin-1 as a satiety molecule in the hypothalamus. Nature 443:709–712

    Article  CAS  Google Scholar 

  • Otte S, Barnikol-Watanabe S, Vorbrüggen G, Hilschmann N (1999) NUCB1, the Drosophila melanogaster homolog of the mammalian EF-hand proteins NEFA and nucleobindin. Mech Dev 86:155–158

    Article  CAS  Google Scholar 

  • Parker J, Bloom SR (2012) Hypothalamic neuropeptides and the regulation of appetite. Neuropharmacology 63:18–30

    Article  CAS  Google Scholar 

  • Ramesh N, Mohan H, Unniappan S (2015) Nucleobindin-1 encodes a nesfatin-1-like peptide that stimulates insulin secretion. Gen Comp Endocrinol 216:182

    Article  CAS  Google Scholar 

  • Ronnestad I, Gomes AS, Murashita K, Angotzi R, Jonsson E, Volkoff H (2017) Appetite-controlling endocrine systems in teleosts. Front Endocrinol 8

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat Protoc 3:1101–1108

    Article  CAS  Google Scholar 

  • Shimizu, H., Ohi., S., Hashimoto, K., Nakata, M., Yamamoto, S., Yoshida, N., Eguchi, H., Kato, I., Inoue, K., Satoh, T., 2009. Peripheral administration of nesfatin-1 reduces food intake in mice: the leptin-independent mechanism. Endocrinology 150, 662–671

  • Stengel A, Goebelstengel M, Wang L, Kato I, Mori M, Taché Y (2012) Nesfatin-1(30-59) but not the N- and C-terminal fragments, nesfatin-1(1-29) and nesfatin-1(60-82) injected intracerebroventricularly decreases dark phase food intake by increasing inter-meal intervals in mice. Peptides 35:143

    Article  CAS  Google Scholar 

  • Sundarrajan L, Blanco AM, Bertucci JI, Ramesh N, Canosa LF, Unniappan S (2016) Nesfatin-1-like peptide encoded in nucleobindin-1 in goldfish is a novel anorexigen modulated by sex steroids, macronutrients and daily rhythm. Sci Rep 6:28377–28377

    Article  CAS  Google Scholar 

  • Tulke S, Williams P, Hellysaz A, Ilegems E, Wendel M, Broberger C (2016) Nucleobindin 1 (NUCB1) is a golgi-resident marker of neurons. Neuroscience 314:179–188

    Article  CAS  Google Scholar 

  • Volkoff H (2016) The neuroendocrine regulation of food intake in fish: a review of current knowledge. Front Neurosci 10

  • Volkoff H, Peter RE (2001) Interactions between orexin A, NPY and galanin in the control of food intake of the goldfish, Carassius auratus. Regul Pept 101:59–72

    Article  CAS  Google Scholar 

  • Volkoff H, Hoskins LJ, Tuziak SM (2010) Influence of intrinsic signals and environmental cues on the endocrine control of feeding in fish: potential application in aquaculture. Gen Comp Endocrinol 167:352–359

    Article  CAS  Google Scholar 

  • Volkoff H, Sabioni RE, Cyrino JE (2016) Appetite regulating factors in dourado, Salminus brasiliensis: cDNA cloning and effects of fasting and feeding on gene expression. Gen Comp Endocrinol 237:34–42

    Article  CAS  Google Scholar 

  • Volkoff H, Sabioni RE, Coutinho LL, Cyrino JEP (2017) Appetite regulating factors in pacu (Piaractus mesopotamicus ): tissue distribution and effects of food quantity and quality on gene expression. Com Biochem Physio A Mol Integr Physiol 203:241–254

    Article  CAS  Google Scholar 

  • Williams P, Tulke S, Ilegems E, Berggren PO, Broberger C (2014) Expression of nucleobindin 1 (NUCB1) in pancreatic islets and other endocrine tissues. Cell Tissue Res 358:331–342

    Article  CAS  Google Scholar 

  • Wu H, Lin F, Chen H, Liu J, Gao Y, Zhang X, Hao J, Chen D, Yuan D, Wang T (2015) Ya-fish (Schizothorax prenanti) spexin: identification, tissue distribution and mRNA expression responses to periprandial and fasting. Fish Physiol Biochem 42:39–49

    Article  Google Scholar 

  • Xue F, Wu Y, Zhao X, Zhao T, Meng Y, Zhao Z, Guo J, Chen W (2016) CHIP mediates down-regulation of nucleobindin-1 in preosteoblast cell line models. Cell Signal 28:1058–1065

    Article  CAS  Google Scholar 

  • Yamada M, Horiguchi K, Umezawa R, Hashimoto K, Satoh T, Ozawa A, Shibusawa N, Monden T, Okada S, Shimizu H (2010) Troglitazone, a ligand of peroxisome proliferator-activated receptor-{gamma}, stabilizes NUCB2 (Nesfatin) mRNA by activating the ERK1/2 pathway: isolation and characterization of the human NUCB2 gene. Endocrinology 151:2494

    Article  CAS  Google Scholar 

  • Yuan D, Zhou C, Wang T, Lin F, Chen H, Wu H, Wei R, Xin Z, Liu J, Gao Y (2014) Molecular characterization and tissue expression of peptide YY in Schizothorax prenanti: effects of periprandial changes and fasting on expression in the hypothalamus. Regul Pept 190:32–38

    Article  Google Scholar 

  • Yuan D, Wei R, Wang T, Wu Y, Lin F, Chen H, Liu J, Gao Y, Zhou C, Chen D (2015) Appetite regulation in Schizothorax prenanti by three CART genes. Gen Comp Endocrinol 224:194–204

    Article  CAS  Google Scholar 

  • Zhang X, Wu Y, Hao J, Zhu J, Tang N, Qi J, Wang S, Wang H, Peng S, Liu J (2016) Intraperitoneal injection urocortin-3 reduces the food intake of Siberian sturgeon (Acipenser baerii). Peptides 85:80–88

    Article  CAS  Google Scholar 

  • Zhang X, Tang N, Qi J, Wang S, Hao J, Wu Y, Chen H, Tian Z, Wang B, Chen D (2017) CCK reduces the food intake mainly through CCK1R in Siberian sturgeon (Acipenser baerii Brandt). Sci Rep 7:12413

    Article  Google Scholar 

  • Zhang X, Gao Y, Tang N, Qi J, Wu Y, Hao J, Wang S, Chen D, Li Z (2018a) One evidence of cocaine- and amphetamine-regulated transcript (CART) has the bidirectional effects on appetite in Siberian sturgeon (Acipenser baerii). Fish Physiol Biochem 44:411–422

    Article  CAS  Google Scholar 

  • Zhang X, Wang S, Chen H, Tang N, Qi J, Wu Y, Hao J, Tian Z, Wang B, Chen D (2018b) The inhibitory effect of NUCB2/nesfatin-1 on appetite regulation of Siberian sturgeon (Acipenser baerii Brandt). Horm Behav 103:111–120

    Article  CAS  Google Scholar 

  • Zhou XH, Xiang X, Chen J (2006) Analysis of the nutritional components in muscle of Schizothorax (Racoma) davidi (Sauvage). Acta Nutrimenta Sinica

  • Zhu P, Tang Y, Fan J, Fang J, Peng X, Cui H (2017) Hematological parameters and blood cell morphology of male and female Schizothorax (Racoma) davidi (Sauvage). J World Aquacult Soc 48

Download references

Acknowledgments

We are very grateful to the company of Runzhao Fisheries (Sichuan, China) for supplying fish.

Funding

This study is supported by grants from the Open Project Program of Key Laboratory of Aquatic Science of Chongqing (klas-2017-01).

Author information

Author notes

  1. Dengyue Yuan and Xin Zhang contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing, China

    Dengyue Yuan

  2. The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao, Shandong, China

    Xin Zhang

  3. The Department of Aquaculture, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan, China

    Bin Wang, Tao Tang & Zhiqiong Li

  4. The Department of Aquaculture, College of Animal Science, Southwest University, Chongqing, China

    Luo Lei, Xingxing Deng & Chaowei Zhou

Authors
  1. Dengyue Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tao Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luo Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xingxing Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chaowei Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhiqiong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dengyue Yuan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yuan, D., Zhang, X., Wang, B. et al. Effects of feeding status on nucb1 and nucb2A mRNA expression in the hypothalamus of Schizothorax davidi. Fish Physiol Biochem 46, 1139–1154 (2020). https://doi.org/10.1007/s10695-020-00780-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00780-1

Keywords

Search

Navigation