Log in

Effects of fasting, temperature, and photoperiod on preproghrelin mRNA expression in Chinese perch

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

Abstract

Preproghrelin, a gut/brain peptide, plays an important role in the regulation of food intake and energy homeostasis in teleost and mammals. In the present study, we obtained the full-length preproghrelin cDNA in Chinese perch. The preproghrelin messenger RNA (mRNA) tissue expression showed that level was much higher in stomach and pituitary than in other tissues. The fasting study showed, after gastric emptying (3–6 h), short-term fasting (6–12 h) increased preproghrelin expression in the stomach. While in the pituitary, fasting reduced preproghrelin expression at 1, 3, 12, and 48 h, presenting state fluctuation of self-adjustment. The temperature study showed that the mRNA expression of preproghrelin was the highest in the brain at 26 °C and highest in the stomach at 32 °C, respectively, with different optimum temperature in these two tissues, reflecting spatiotemporal differences of regulation by central nervous system and peripheral organs. The photoperiod study showed that normal light (11 h of lightness and 13 h of darkness) led to highest preproghrelin expression, both in the brain and in the stomach, than continuous light or continuous dark, proving food intake is adapted to natural photoperiod or normal light in this study. These results all indicated that tissue-specific preproghrelin expression of Chinese perch could be significantly affected by environmental factors. Short-term fasting of 6 h after gastric emptying, 26 °C, and normal light led to higher preproghrelin expression, which indicated potential appetite increase in Chinese perch.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amole N, Unniappan S (2009) Fasting induces preproghrelin mRNA expression in the brain and gut of zebrafish, Danio rerio. Gen Comp Endocrinol 161:133–137

    Article  CAS  PubMed  Google Scholar 

  • Ariyasu H, Takaya K, Tagami T, Ogawa Y, Hosoda K, Akamizu T, Suda M, Koh T, Natsui K, Toyooka S, Shirakami G, Usui T, Shimatsu A, Doi K, Hosoda H, Kojima M, Kanqawa K, Nakao K (2001) Stomach is a major source of circulating ghrelin, and feeding state determines plasma ghrelin-like immunoreactivity levels in humans. J Clin Endocrinol Metab 86:4753–4758

    Article  CAS  PubMed  Google Scholar 

  • Bednarek MA, Feighner SD, Pong SS, McKee KK, Hreniuk DL, Silva MV, Warren VA, Howard AD, Van Der Ploeq LH, Heck JV (2000) Structure-function studies on the new growth hormone-releasing peptide, ghrelin: minimal sequence of ghrelin necessary for activation of growth hormone secretagogue receptor 1a. J Med Chem 43:4370–4376

    Article  CAS  PubMed  Google Scholar 

  • Bendiksen E, Jobling M, Arnesen A (2002) Feed intake of Atlantic salmon parr Salmo salar L. in relation to temperature and feed composition. Aquac Res 33:525–532

    Article  Google Scholar 

  • Bernier NJ, Peter RE (2001) The hypothalamic–pituitary–interrenal axis and the control of food intake in teleost fish. Comp Biochem Phys B 129(2):639–644

    Article  CAS  Google Scholar 

  • Cai L, Liu G, Taupier R, Fang M, Johnson D, Tu Z, Huang Y (2014) Effect of temperature on swimming performance of juvenile Schizothorax prenanti. Fish Physiolo Biochem 40(2):491–498

    Article  CAS  Google Scholar 

  • Chen T, Tang Z, Yan A, Li W, Lin H (2008) Molecular cloning and mRNA expression analysis of two GH secretagogue receptor transcripts in orange-spotted grouper (Epinephelus coioides). J Endocrinol 199(2):253–265

    Article  CAS  PubMed  Google Scholar 

  • Chiang IK (1959) On the biology of mandarin fish, Siniperca chuatsi of Liang-Tze Lake. Acta Hydrobiol Sin 3:375–385

    Google Scholar 

  • Feng KE, Zhang GR, Wei KJ, **ong BX (2013) Molecular cloning, tissue distribution, and ontogenetic expression of ghrelin and regulation of expression by fasting and refeeding in the grass carp (Ctenopharyngodon idellus). J Exp Zool A 319:202–212

    Article  CAS  Google Scholar 

  • Frøiland E, Murashita K, Jørgensen EH, Kurokawa T (2010) Leptin and ghrelin in anadromous Arctic charr: cloning and change in expressions during a seasonal feeding cycle. Gen Comp Endocr 165(1):136–143

    Article  PubMed  Google Scholar 

  • Gnanapavan S, Kola B, Bustin SA, Morris DG, McGee P, Fairclough P, Bhattacharya S, Carpenter R, Grossman AB, Korbonits M (2002) The tissue distribution of the mRNA of ghrelin and subtypes of its receptor, GHS-R, in humans. J Clin Endocrinol Metab 87:2988–2988

    Article  CAS  PubMed  Google Scholar 

  • Hevrøy EM, Waagbø R, Torstensen BE, Takle H, Stubhaug I, Jørgensen SM, Torgersen T, Tvenning L, Susort S, Breck O, Hansen T (2012) Ghrelin is involved in voluntary anorexia in Atlantic salmon raised at elevated sea temperatures. Gen Comp Endocrinol 175:118–134

    Article  PubMed  Google Scholar 

  • Jönsson E, Forsman A, Einarsdottir IE, Kaiya H, Ruohonen K, Björnsson BT (2007) Plasma ghrelin levels in rainbow trout in response to fasting, feeding and food composition, and effects of ghrelin on voluntary food intake. Comp Biochem Phys A 147:1116–1124

    Article  Google Scholar 

  • Kaiya H, Kojima M, Hosoda H, Moriyama S, Takahashi A, Kawauchi H, Kangawa K (2003a) Peptide purification, complementary deoxyribonucleic acid (DNA) and genomic DNA cloning, and functional characterization of ghrelin in rainbow trout. Endocrinology 144:5215–5226

    Article  CAS  PubMed  Google Scholar 

  • Kaiya H, Kojima M, Hosoda H, Riley LG, Hirano T, Grau EG, Kangawa K (2003b) Amidated fish ghrelin: purification, cDNA cloning in the Japanese eel and its biological activity. J Endocrinol 176:415–423

    Article  CAS  PubMed  Google Scholar 

  • Kaiya H, Kojima M, Hosoda H, Riley LG, Hirano T, Grau EG, Kangawa K (2003c) Identification of tilapia ghrelin and its effects on growth hormone and prolactin release in the tilapia, Oreochromis mossambicus. Comp Biochem Phys B 135:421–429

    Article  Google Scholar 

  • Kaiya H, Small BC, Bilodeau AL, Shepherd BS, Kojima M, Hosoda H, Kangawa K (2005) Purification, cDNA cloning, and characterization of ghrelin in channel catfish, Ictalurus punctatus. Gen Comp Endocr 143:201–210

    Article  CAS  PubMed  Google Scholar 

  • Kaiya H, Tsukada T, Yuge S, Mondo H, Kangawa K, Takei Y (2006) Identification of eel ghrelin in plasma and stomach by radioimmunoassay and histochemistry. Gen Comp Endocrinol 148:375–382

    Article  CAS  PubMed  Google Scholar 

  • Kaiya H, Miyazato M, Kangawa K, Peter RE, Unniappan S (2008) Ghrelin: a multifunctional hormone in non-mammalian vertebrates. Comp Biochem Phys A 149:109–128

    Article  Google Scholar 

  • Kang KS, Yahashi S, Matsuda K (2011a) Central and peripheral effects of ghrelin on energy balance, food intake and lipid metabolism in teleost fish. Peptides 32:2242–2247

    Article  CAS  PubMed  Google Scholar 

  • Kang KS, Yahashi S, Matsuda K (2011b) The effects of ghrelin on energy balance and psychomotor activity in a goldfish model: an overview. Int J Peptides 2011:1–9

    Article  Google Scholar 

  • Kawakoshi A, Kaiya H, Riley LG, Hirano T, Grau EG, Miyazato M, Kangawa K (2007) Identification of a ghrelin-like peptide in two species of shark, Sphyrna lewini and Carcharhinus melanopterus. Gen Comp Endocr 151(3):259–268

    Article  CAS  PubMed  Google Scholar 

  • Kohbara J, Hidaka I, Kuriyama I, Yamashita M, Ichikawa M, Furukawa K, Aida K, Sanchez-Vazquez FJ, Tabata M (2000) Nocturnal/diurnal demand-feeding pattern of yellowtail Seriola quinqueradiata under different kee** conditions. Fish Sci 66:955–962

    Article  CAS  Google Scholar 

  • Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402:656–660

    Article  CAS  PubMed  Google Scholar 

  • Kono T, Kitao Y, Sonoda K, Nomoto R, Mekata T, Sakai M (2008) Identification and expression analysis of ghrelin gene in common carp Cyprinus carpio. Fish Sci 74:603–612

    Article  CAS  Google Scholar 

  • Kubitza F, Lovshin LL (1999) Formulated diets, feeding strategies, and cannibalism control during intensive culture of juvenile carnivorous fishes. Rev Fish Sci 7:1–22

    Article  Google Scholar 

  • Kullgren A, Jutfelt F, Fontanillas R, Sundell K, Samuelsson L, Wiklander K, Kling P, Koppe W, Joakim Larsson DG, Björnsson TB, Jönsson E (2013) The impact of temperature on the metabolome and endocrine metabolic signals in Atlantic salmon (Salmo salar). Comp Biochem Phys A 164:44–53

    Article  CAS  Google Scholar 

  • Liang XF, Oku H, Ogata HY, Liu J, He X (2001) Weaning Chinese perch Siniperca chuatsi (Basilewsky) onto artificial diets based upon its specific sensory modality in feeding. Aquac Res 36:1588–1594

    Google Scholar 

  • Liang XF, Lin XT, Li SQ, Liu JK (2008) Impact of environmental and innate factors on the food habit of Chinese perch Siniperca chuatsi (Basilewsky) (Percichthyidae). Aquac Res 39:150–157

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Matsuda K, Miura T, Kaiya H, Maruyama K, Shimakura SI, Uchiyama M, Shioda S (2006) Regulation of food intake by acyl and des-acyl ghrelins in the goldfish. Peptides 27(9):2321–2325

    Article  CAS  PubMed  Google Scholar 

  • Matteri RL (2001) Overview of central targets for appetite regulation. J Anim Sci 79(E-Suppl):E148–E158

    Article  Google Scholar 

  • Miura T, Maruyama K, Shimakura SI, Kaiya H, Uchiyama M, Kangawa K, Shioda S, Matsuda K (2006) Neuropeptide Y mediates ghrelin-induced feeding in the goldfish, Carassius auratus. Neurosci Lett 407:279–283

    Article  CAS  PubMed  Google Scholar 

  • Murashita K, Kurokawa T, Nilsen TO, Rønnestad I (2009) Ghrelin, cholecystokinin, and peptide YY in Atlantic salmon (Salmo salar): molecular cloning and tissue expression. Gen Comp Endocr 160(3):223–235

    Article  CAS  PubMed  Google Scholar 

  • Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S (2001) A role for ghrelin in the central regulation of feeding. Nature 409:194–198

    Article  CAS  PubMed  Google Scholar 

  • Nieminen P, Mustonen AM, Hyvärinen H (2003) Fasting reduces plasma leptin- and ghrelin-immunoreactive peptide concentrations of the burbot (Lota lota) at 2 °C but not at 10 °C. Zool Sci 20:1109–1115

    Article  CAS  PubMed  Google Scholar 

  • Parhar IS, Sato H, Sakuma Y (2003) Ghrelin gene in cichlid fish is modulated by sex and development. Biochem Biophys Res Commun 305:169–175

    Article  CAS  PubMed  Google Scholar 

  • Peddu SC, Breves JP, Kaiya H, Grau EG, Riley LG (2009) Pre-and postprandial effects on ghrelin signaling in the brain and on the GH/IGF-I axis in the Mozambique tilapia (Oreochromis mossambicus). Gen Comp Endocr 161(3):412–418

    Article  CAS  PubMed  Google Scholar 

  • Pfaff, D (1969) Sex differences in food intake changes following pituitary growth hormone or prolactin injections. In Proceedings of the Annual Convention of the American Psychological Association. American Psychological Association.

  • Picha ME, Strom CN, Riley LG, Walker AA, Won ET, Johnstone WM, Borski RJ (2009) Plasma ghrelin and growth hormone regulation in response to metabolic state in hybrid striped bass: effects of feeding, ghrelin and insulin-like growth factor-I on in vivo and in vitro GH secretion. Gen Comp Endocr 161:365–372

    Article  CAS  PubMed  Google Scholar 

  • Riley LG, Fox BK, Kaiya H, Hirano T, Grau EG (2005) Long-term treatment of ghrelin stimulates feeding, fat deposition, and alters the GH/IGF-I axis in the tilapia, Oreochromis mossambicus. Gen Comp Endocr 142:234–240

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Vazquez FJ, Azzaydi M, Martinez FJ, Zamora S, Madrid JA (1998) Annual rhythms of demand-feeding activity in sea bass: evidence of a seasonal phase inversion of the diel feeding pattern. Chronobiol Int 15:607–622

    Article  CAS  PubMed  Google Scholar 

  • Suda A, Kaiya H, Nikaido H, Shiozawa S, Mishiro K, Ando H (2012) Identification and gene expression analyses of ghrelin in the stomach of Pacific bluefin tuna (Thunnus orientalis). Gen Comp Endocrinol 178:89–97

    Article  CAS  PubMed  Google Scholar 

  • Sunuma T, Amano M, Yamanome T, Furukawa K, Yamamori K (2007) Self-feeding activity of a pleuronectiform fish, the barfin flounder. Aquaculture 270:566–569

    Article  Google Scholar 

  • Terova G, Rimoldi S, Bernardini G, Gornati R, Saroglia M (2008) Sea bass ghrelin: molecular cloning and mRNA quantification during fasting and refeeding. Gen Comp Endocrinol 155:341–351

    Article  CAS  PubMed  Google Scholar 

  • Unniappan S, Lin X, Cervini L, Rivier J, Kaiya H, Kangawa K, Peter RE (2002) Goldfish ghrelin: molecular characterization of the complementary deoxyribonucleic acid, partial gene structure and evidence for its stimulatory role in food intake. Endocrinology 143:4143–4146

    Article  CAS  PubMed  Google Scholar 

  • Unniappan S, Canosa LF, Peter RE (2004) Orexigenic actions of ghrelin in goldfish: feeding-induced changes in brain and gut mRNA expression and serum levels, and responses to central and peripheral injections. Neuroendocrinology 79:100–108

    Article  CAS  PubMed  Google Scholar 

  • Volkoff H, Xu M, MacDonald E, Hoskins L (2009) Aspects of the hormonal regulation of appetite in fish with emphasis on goldfish, Atlantic cod and winter flounder: notes on actions and responses to nutritional, environmental and reproductive changes. Comp Biochem Physiol A 153:8–12

    Article  Google Scholar 

  • Wang G, Lee HM, Englander E, Greeley GH (2002) Ghrelin not just another stomach hormone. Regul Peptides 105(2):75–81

    Article  CAS  Google Scholar 

  • Wen LY, Tan YJ, Wang W (1998) Effects of water temperature on feeding, growth and mortality of grass carp fingerlings. J Fish China 22:371–374

    Google Scholar 

  • Wren AM, Small CJ, Ward HL, Murphy KG, Dakin CL, Taheri S, Bloom SR (2000) The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology 141:4325–4328

    Article  CAS  PubMed  Google Scholar 

  • Xu M, Volkoff H (2009) Molecular characterization of ghrelin and gastrin-releasing peptide in Atlantic cod (Gadus morhua): cloning, localization, developmental profile and role in food intake regulation. Gen Comp Endocrinol 160:250–258

    Article  CAS  PubMed  Google Scholar 

  • Yeung CM, Chan CB, Woo NY, Cheng CH (2006) Sea bream ghrelin: cDNA cloning, genomic organization and promoter studies. J Endocrinol 189:365–379

    Article  CAS  PubMed  Google Scholar 

  • Zhou C, Zhang X, Liu T, Wei R, Yuan D, Li Z (2012) Cloning and prokaryotic expression of ghrelin gene in crucian carp (Carassius auratus). Afr J Microbiol Res 6(24):5222–5228

    CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (31272641), the Key Projects in the National Science & Technology Pillar Program (2012BAD25B04), and the Fundamental Research Funds for the Central Universities (2662015PY041 and 2015BQ040).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xu-fang Liang.

Electronic supplementary material

.

ESM 1

(DOCX 625 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, Y., Zhao, C., Liang, Xf. et al. Effects of fasting, temperature, and photoperiod on preproghrelin mRNA expression in Chinese perch. Fish Physiol Biochem 43, 803–812 (2017). https://doi.org/10.1007/s10695-016-0335-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0335-y

Keywords

Navigation