Skip to main content
SpringerLink
Log in

A cross-talk between leptin and 17β-estradiol in vitellogenin synthesis in rainbow trout Oncorhynchus mykiss liver

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

Abstract

The existence of nutritional and energy reserves is fundamental for fish female fertility, so that the existence of a correlation between metabolic reserves and reproductive capacity is suggested. Leptin regulates body weight and energy homeostasis. Estradiol induces the synthesis of vitellogenin, a phospholipoglycoprotein produced by the liver and taken up by the growing oocytes. The objective of this study was to investigate the possible existence of a crosstalk between 17β-estradiol (E2) and leptin in the modulation of E2-induced vtg in the rainbow trout Oncorhynchus mykiss. Liver slices were incubated with recombinant trout leptin (rt-lep) at three different concentrations (1–10–100 ng/ml). rt-lep brought about the decrease of E2-induced vtg secretion in the medium and the down-regulation of vtg mRNA expression. Moreover, rt-lep stimulated the lipase activity and diminished the liver fatty acid content. The combined employment of signal transduction inhibitors and the analysis of signal transduction phosphorylated factors revealed that rt-lep effect on E2-induced vtg occurred through the activation of phosphodiesterase, protein kinase C, MAP kinases, and protein kinase A. In conclusion, our study suggests that leptin influences E2-induced vtg synthesis in the rainbow trout Oncorhynchus mykiss by modifying both the protein and the lipid components.

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
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Akhavan SR, Salati AP, Falahatkar B, Jalali SAH (2016) Changes of vitellogenin and Lipase in captive Sterlet sturgeon Acipenser ruthenus females during previtellogenesis to early atresia. Fish Physiol Biochem 42(3):967–978

    CAS  PubMed  Google Scholar 

  • Babin PJ, Bogerd J, Kooiman FP, Van Marrewijk WJA, Van der Horst DJ (1999) Apolipophorin II/I, Apolipoprotein B, Vitellogenin, and Microsomal Triglyceride Transfer Protein Genes Are Derived from a Common Ancestor. J Mol Evol 49:150–160

    CAS  PubMed  Google Scholar 

  • Bailey GS, Williams DE, Hendricks JD (1996) Fish Models for Environmental Carcinogenesis: The Rainbow Trout. Environ Health Perspect 104:5–21

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baker HJ, Shapiro DJ (1977) Kinetics of estrogen induction of Xenopus laevis vitellogenin messenger RNA as measured by hybridization to complementary DNA. J Biol Chem 252(23):8428–8434

    CAS  PubMed  Google Scholar 

  • Blundell JE, Goodson S, Halford JCG (2001) Regulation of appetite: role of leptin in signalling systems for drive and satiety. Int J Obes 25:S29–S34

    CAS  PubMed  Google Scholar 

  • Chan L (1992) Apolipoprotein B, the major protein component of triglyceride-rich and low density lipoproteins. J Biol Chem 267:25621–25624

    CAS  PubMed  Google Scholar 

  • Chen T, Chunhua RC, Jiang X, Zhang L, Li H, Huang W, Hu C (2018) Mechanisms for type-II vitellogenesis inhibiting hormone suppression of vitellogenin transcription in shrimp hepatopancreas: Crosstalk of GC/cGMP pathway with different MAPK-dependent cascades. PLoS One 13(3):e0194459. https://doi.org/10.1371/journal.pone.0194459

    PubMed  PubMed Central  Google Scholar 

  • Chisada S, Kurokawa T, Murashita K, Rønnestad I, Taniguchi Y, Toyoda A, Sakaki Y, Takeda S, Yoshiura Y (2014) Leptin receptor-deficient (knockout) medaka, Oryzias latipes, show chronical up-regulated levels of orexigenic neuropeptides, elevated food intake and stage specific effects on growth and fat allocation. Gen Comp Endocrinol 195:9–20

    CAS  Google Scholar 

  • Choi YJ, Kim NN, Shin HS, Choi CY (2014) The Expression of Leptin, Estrogen Receptors, and Vitellogenin mRNAs in Migrating Female Chum Salmon, Oncorhynchus keta: The Effects of Hypo-osmotic Environmental Changes. Asian Australas J Anim Sci 27:479–487

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clegg DJ, Brown LM, Woods SC, Benoit SC (2006) Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 55:978–987

    CAS  PubMed  Google Scholar 

  • Cleveland BM, Manor ML (2015) Effects of phytoestrogens on growth-related and lipogenic genes in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol C 170:28–37

    CAS  Google Scholar 

  • Coccia E, Varricchio E, Vito P, Turchini GM, Francis DS, Paolucci M (2014) Fatty acid-specific alterations in leptin, PPARα, and CPT-1 gene expression in the rainbow trout. Lipids 49:1033–1046

    CAS  PubMed  Google Scholar 

  • Coccia E, Imperatore R, Orso G, Melck D, Varricchio E, Volpe MG, Paolucci M (2019) Explants of Oncorhynchus mykiss intestine to detect bioactive molecules uptake and metabolic effects: Applications in aquaculture. Aquaculture 506:193–204

    CAS  Google Scholar 

  • Costantini S, Parrillo L, Guerriero E, Melck D, Colonna G, Volpe MG, Paolucci M (2018) 1H-NMR metabolomic profiling of the crayfish Astacus leptodactylus subjected to polyphenol-enriched diets. Aquac Nutr 24:524–538

    CAS  Google Scholar 

  • Deck CA, Honeycutt JL, Cheung E, Reynolds HM, Borski RJ (2017) Assessing the Functional Role of Leptin in energy Homeostasis and the Stress Response in vertebrates. Front Endocrinol 8:63. https://doi.org/10.3389/fendo.2017.00063

    Article  Google Scholar 

  • Degani D (2016) Oogenesis Control in Multi-Spawning Blue Gourami (Trichogaster Trichopterus) as a Model For the Anabantidae Family. Int J Sci Res 5:179–184

    Google Scholar 

  • Degani G, Din SY, Hurvitz A (2017) Transcription of Insulin-like Growth Factor Receptor in Russian Sturgeon (Acipenser gueldenstaedtii) Ovary during Oogenesis. Univers J Agric Res 5:119–124

    Google Scholar 

  • Ding W, Cao L, Cao Z, Bing X, Zhao F (2016) Molecular characterization and expression profile of the estrogen receptor α gene during different reproductive phases in Monopterus albus. Sci Rep 6:27924. https://doi.org/10.1038/srep27924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duncan RE, Maryam AM, Jaworski K, Sarkadi-Nagy E, Sul HS (2007) Regulation of Lipolysis in Adipocytes. Annu Rev Nutr 27:79–101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Emmerson J, Korsgaard B, Petersen I (1979) Dose response kinetics of serum vitellogenin, liver DNA, RNA, protein and lipid after induction by estradiol-17 beta in male flounders (Platichthys flesus L.). Comp Biochem Physiol B 63:1–6

    CAS  PubMed  Google Scholar 

  • Etgen AM, Acosta-Martinez M (2003) Participation of Growth Factor Signal Transduction Pathways in Estradiol Facilitation of Female Reproductive Behavior. Endocrinology 144:3828–3835

    CAS  PubMed  Google Scholar 

  • FAO (2018) The State of World Fisheries and Aquaculture 2018 - Meeting the sustainable development goals. Rome. http://www.fao.org/3/i9540en/i9540en.pdf

  • Farrell RE Jr (2009) RNA Methodologies: Laboratory Guide for Isolation and Characterization. Elsevier Science, Amsterdam

    Google Scholar 

  • Francis DS, Thanuthong T, Senadheera SPSD, Paolucci M, Coccia E, De Silva SS, Turchini GM (2014) n-3 LC-PUFA deposition efficiency and appetite regulating hormones are modulated by the dietary lipid source during rainbow trout growout and finishing periods. Fish Physiol Biochem 40:577–593

    CAS  PubMed  Google Scholar 

  • Fruhbeck G (2006) Intracellular signalling pathways activated by leptin. Biochem J 393:7–20

    CAS  PubMed  Google Scholar 

  • Gao Q, Horvath TL (2008) Cross-talk between estrogen and leptin signaling in the hypothalamus. Am J Physiol Endocrinol Metab 294:E817–E826

    CAS  PubMed  Google Scholar 

  • Gellissen G (2004) Production of Recombinant Proteins: Novel Microbial and Eukaryotic Expression Systems. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim

    Google Scholar 

  • Gorissen M, Flik G (2014) Leptin in teleostean fish, towards the origins of leptin physiology. J Chem Neuroanat 6:200–206

    Google Scholar 

  • Green CD, Tata JR (1976) Direct induction by estradiol of vitellogenin synthesis in organ cultures of male Xenopus laevis liver. Cell 7:131–139

    CAS  PubMed  Google Scholar 

  • Grunow B, Wenzel J, Terlau H, Langner S, Gebert M, Kruse C (2011) In vitro Developed Spontaneously Contracting Cardiomyocytes from Rainbow Trout as a Model System for Human Heart Research. Cell Physiol Biochem 27:1–12

    CAS  PubMed  Google Scholar 

  • Guzmán M, Norberg B, Ramos J, Mylonas CC, Mañanós EL (2008) Vitellogenin, steroid plasma levels and spawning performance of cultured female Senegalese sole (Solea senegalensis). Gen Comp Endocrinol 156:285–297

    PubMed  Google Scholar 

  • Huynh FK, Neumann UH, Wang Y, Rodrigues B, Kieffer TJ, Covey SD (2013) A Role for Hepatic Leptin Signaling in Lipid Metabolism via Altered Very Low Density Lipoprotein Composition and Liver Lipase Activity in Mice. Hepatology 57:543–554

    CAS  PubMed  Google Scholar 

  • Imperatore R, D'Angelo L, De Girolamo P, Cristino L, Paolucci M (2019) Identification of Orexin and Endocannabinoid Receptors in Adult Zebrafish Using Immunoperoxidase and Immunofluorescence Methods. Jove 148. https://doi.org/10.3791/59308

  • James G, Witten D, Hastie T, Tibshirani R(2013) An Introduction to Statistical Learning: with Applications in R, Springer Texts in Statistics 103, https://doi.org/10.1007/978-1-4614-7138-71, © Springer Science+Business Media New York 2013

  • Jorgensen EH, Bernier NJ, Maule AG, Vijayan MM (2016) Effect of long-term fasting and a subsequent meal on mRNA abundances of hypothalamic appetite regulators, central and peripheral leptin expression and plasma leptin levels in rainbow trout. Peptides 86:162–170

    PubMed  Google Scholar 

  • Kurokawa T, Uji S, Suzuki T (2005) Identification of cDNA coding for a homologue to mammalian leptin from puffer fish, Takifugu rubripes. Peptides 26:45–750

    Google Scholar 

  • Li GG, Liang XF, Guangzhao QX, Yu Y, Lai K (2010) Gene structure, recombinant expression and functional characterization of grass carp leptin. Gen Comp Endocrinol 166:117–127

    CAS  PubMed  Google Scholar 

  • Londraville RL, Prokop JW, Duff RJ, Liu Q, Tuttle M (2017) On the Molecular evolution of Leptin, Leptin receptor, and endospanin Leptin Receptor and Endospanin. Hypothesis and theory. https://doi.org/10.3389/fendo.2017.00058

  • Luo G, Zhang X, Nilsson-Ehle P, Xu N (2004) Apolipoprotein M. Lipids Health Dis 3:21

    PubMed  PubMed Central  Google Scholar 

  • Luo G, Hurtig M, Zhang X, Nilsson-Ehle P, Xu N (2005) Regular paperLeptin inhibits apolipoprotein M transcription and secretion inhuman hepatoma cell line, HepG2 cells. Biochim Biophys Acta 1734:198–202

    CAS  PubMed  Google Scholar 

  • Mahmood T, Yang P-C (2012) Western Blot: Technique, Theory, and Trouble Shooting. N Am J Med Sci 4:429–434

    PubMed  PubMed Central  Google Scholar 

  • Mariano G, Terrazzano G, Coccia E, Vito P, Varricchio E, Paolucci M (2013) Effects of recombinant trout leptin in superoxide production and NF-kappaB/ MAPK phosphorylation in blood leukocytes. Peptides 48:59–69

    CAS  PubMed  Google Scholar 

  • Marino M, Acconcia F, Bresciani F, Weisz A, Trentalance A (2002) Distinct Nongenomic Signal Transduction Pathways Controlled by 17β-Estradiol Regulate DNA Synthesis and Cyclin D1 Gene Transcription in HepG2 Cells. Mol Biol Cell 13:3720–3729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matyash V, Geier C, Henske A, Mukherjee S, Hirsh D, Thiele C, Grant B, Maxfield FR, Kurzchalia TV (2001) Distribution and Transport of Cholesterol in Caenorhabditis elegans. Mol Biol Cell 12:1725–1736

    CAS  PubMed  PubMed Central  Google Scholar 

  • Michalakis K, Mintziori G, Kaprara A, Tarlatzis BC, Goulis DG (2013) The complex interaction between obesity, metabolic syndrome and reproductive axis: A narrative review. Metabolism 62:457–478

    CAS  PubMed  Google Scholar 

  • Morash AJ, Kajimura M, McClelland GB (2008) Intertissue regulation of carnitine palmitoyl transferase I (CPTI): Mitochondrial membrane properties and gene expression in rainbow trout (Oncorhynchus mykiss). Biochim Biophys Acta 1778:1382–1389

    CAS  PubMed  Google Scholar 

  • Muoio DM, Dohm GL (2002) Peripheral metabolic actions of leptin. Best Pract Res Clin Endocrinol Metab 16:653–666

    CAS  PubMed  Google Scholar 

  • Murashita K, Uji S, Yamamoto T, Rønnestad I, Kurokawa T (2008) Production of recombinant leptin and its effects on food intake in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 150:377–384

    Google Scholar 

  • Mustonen AM, Nieminen P, Hyvärinen H (2002) Leptin, ghrelin, and energy metabolism of the spawning burbot (Lota lota, L.). J Exp Zool 293:119–126

    CAS  PubMed  Google Scholar 

  • Nagasaka R, Okamoto N, Ushio H (2006) Increased leptin may be involved in the short life span of ayu (Plecoglossus altivelis). J Exp Zool Part A 305:507–512

    Google Scholar 

  • Nagler JJ, Idler DR (1990) Ovarian uptake of vitellogenin and another very high density lipoprotein in winter flounder (Pseudopleuronectes americanus) and their relationship with yolk proteins. Biochem Cell Biol 68:330–335

    CAS  Google Scholar 

  • Nagler JJ, Ruby SM, Idler DI, So YP (1987) Serum phosphoprotein phosphorus and calcium levels as reproductive indicators of Vg in highly vitellogenic mature female and estradiol-injected immature rainbow trout. Can J Zool 65:2421–2425

    CAS  Google Scholar 

  • Ng TB, WooNYS TPPL, Au CYW (1984) Changes in metabolism and hepatic ultrastructure induced by estradiol and testosterone in immature female Epinephelus akaara (Teleostei, Serranidae). Cell Tissue Res 236:651–659

    CAS  PubMed  Google Scholar 

  • Norris DO (1996) In: Norris DO (ed) Vertebrate endocrinology. Academic Press, London

    Google Scholar 

  • Olofsson SO, Boren J (2005) Apolipoprotein B: a clinically important apolipoprotein which assembles atherogenic lipoproteins and promotes the development of atherosclerosis. JIM 258:395–410

    CAS  Google Scholar 

  • Otis JP, Zeituni EM, Thierer JH, Anderson JL, Brown AC, Boehm ED, Cerchione DM, Ceasrine AM, Avraham-Davidi I, Tempelhof H, Yaniv K, Farber SA (2015) Zebrafish as a model for apolipoprotein biology: comprehensive expression analysis and a role for ApoA-IV in regulating food intake. Dis Model Mech 8:295–309

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park H-K, Ahima RS (2014) Leptin signaling. F1000Prime Reports 6:73

    PubMed  PubMed Central  Google Scholar 

  • Patino R, Sullivan CV (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26:57–70

    CAS  Google Scholar 

  • Pérez L, Peñaranda DS, Dufour S, Baloche S, Palstra AP, Van Den Thillart GEEJM, Asturiano JF (2011) Influence of temperature regime on endocrine parameters and vitellogenesis during experimental maturation of European eel (Anguilla anguilla) females. Gen Comp Endocrinol 174:51–59

    PubMed  Google Scholar 

  • Procaccini C, Lourenco EV, Matarese G, La Cava A (2009) Leptin signaling: A key pathway in immune responses. Curr Signal Transduct Ther 4:22–30

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prokop JW, Duff RJ, Ball HC, Copeland DL, Londraville RL (2012) Leptin and leptin receptor: analysis of a structure to function relationship in interaction and evolution from humans to fish. Peptides 38:326–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reading BJ, Sullivan CV (2017) Vitellogenesis in Fishes.https://doi.org/10.1016/B978-0-12-809633-8.03076-4

    Google Scholar 

  • Robertson SA, Leinninger GM, Myers MG Jr (2008) Molecular and Neural Mediators of Leptin Action. Physiol Behav 94:637–642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Shapiro DJ (1982) Steroid hormone regulation of vitellogenin gene expression. CRC Crit Rev Biochem 12:187–203

    CAS  PubMed  Google Scholar 

  • Shilling AD, Williams DE (2000) The non-aromatizable androgen, dihydrotestosterone, induces antiestrogenic responses in the rainbow trout. J Steroid Biochem Mol Biol 74:187–194

    CAS  PubMed  Google Scholar 

  • Silversand C, Haux C (1995) Fatty acid composition of vitellogenin from four teleost species. Comp Physiol B 164:593–599

    CAS  Google Scholar 

  • Solinas G, Becattini B (2017) JNK at the crossroad of obesity, insulin resistance, and cell stress response. Mol Metab 6:174–184

    CAS  PubMed  Google Scholar 

  • Song YF, Wu K, Tan XY, Zhang LH, Zhuo MQ, Pan YX, Chen QL (2015) Effects of recombinant human leptin administration on hepatic lipid metabolism in yellow catfish Pelteobagrus fulvidraco: in vivo and in vitro studies. Gen Comp Endocrinol 212:92–99

    CAS  PubMed  Google Scholar 

  • Tanaka H, Kagawa H, Ohta H, Unuma T, Nomura K (2003) The first production of glass eel in captivity: fish reproductive physiology facilitates great progress in aquaculture. Fish Physiol Biochem 28:493–497

    Google Scholar 

  • Trombley S, Rocha A, Schmitz M (2015) Sex steroids stimulate leptin gene expression in Atlantic salmon parr hepatocytes in vitro. Gen Comp Endocrinol 221:156–164

    CAS  PubMed  Google Scholar 

  • Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, Lin J, Livny M, Mading S, Maziuk D, Miller Z, Nakatani E, Schulte CF, Tolmie DE, Wenger RK, Yao H, Markley JL (2008) BioMagResBank. Nucleic Acids Res 36:D402–D408

    PubMed  PubMed Central  Google Scholar 

  • Williams DE (2012) The rainbow trout liver cancer model: Response to environmental chemicals and studies on promotion and chemoprevention. Comp Biochem Physiol C 155:121–127

    CAS  Google Scholar 

  • Wu K, Tan XY, Xu YH, Shi X, Fan YF, Li DD (2017) JAK family members: molecular cloning, expression profiles and their roles in leptin influencing lipid metabolism in Synechogobius hasta. Comp Biochem Physiol B 203:122–131

    CAS  PubMed  Google Scholar 

  • Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555–556

    CAS  PubMed  Google Scholar 

  • Xia J, Sinelnikov I, Han B, Wishart DS (2015) MetaboAnalyst 3.0 - making metabolomics more meaningful. Nucleic Acids Res 43:W251–W257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Faulkner LD, Hill JW (2012) Cross-talk between metabolism and reproduction: the role of POMC and SF1 neurons. Front Endocrinol 2:98. https://doi.org/10.3389/fendo.2011.00098

    Article  Google Scholar 

  • Yan AF, Chen T, Chen S, Tang DS, Liu F, Jiang X, Huang W, Ren C, Hu C (2016) Signal transduction mechanism for glucagoninduced leptin gene expression in goldfish liver. Int J Biol Sci 12:1544–1554

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu RMK, Chu DLH, Tan T, Tsun LVW, Chan AKC, Giesy JP, Cheng SH, Wu RSS, Kong RYC (2012) Leptin-Mediated Modulation of Steroidogenic Gene Expression in Hypoxic Zebrafish Embryos: Implications for the Disruption of Sex Steroids. Environ Sci Technol 46:9112–9119

    CAS  PubMed  Google Scholar 

  • Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432

    CAS  Google Scholar 

  • Zohar Y, Muñoz-Cueto JA, Elizur A, Kah O (2010) Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165:438–455

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Sciences and Technologies, University of Sannio, Via Port’Arsa, 11, 82100, Benevento, Italy

    Marina Paolucci, Elena Coccia, Roberta Imperatore & Ettore Varricchio

Authors
  1. Marina Paolucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena Coccia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roberta Imperatore
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ettore Varricchio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marina Paolucci.

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

Paolucci, M., Coccia, E., Imperatore, R. et al. A cross-talk between leptin and 17β-estradiol in vitellogenin synthesis in rainbow trout Oncorhynchus mykiss liver. Fish Physiol Biochem 46, 331–344 (2020). https://doi.org/10.1007/s10695-019-00720-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00720-8

Keywords

Search

Navigation