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Sex steroids stimulate leptin gene expression in Atlantic salmon parr hepatocytes in vitro
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Comparative Physiology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Comparative Physiology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Comparative Physiology.
2015 (English)In: General and Comparative Endocrinology, ISSN 0016-6480, E-ISSN 1095-6840, Vol. 221, 156-164 p.Article in journal (Refereed) Published
Abstract [en]

In mammals, leptin plays an important role in puberty and reproduction and leptin is regulated by sex steroids. Elevated leptin levels have been associated with sexual maturation in some teleosts such as Atlantic salmon. In the present study, primary cultures of Atlantic salmon hepatocytes were used to investigate the direct effects of different sex steroids on expression of the two salmon leptin-a genes, lepa1 and lepa2. Testosterone (T) stimulated both lepa1 and lepa2 in a dose dependent manner after four days of incubation. The stimulatory effect of T on leptin expression was not prevented by co-incubation with the aromatase inhibitor fadrozole, indicating a direct androgen effect on transcription. The non-aromatizable androgen 11-ketotestosterone (11-KT), which is the main androgen in fish, was generally slightly less potent than T in stimulating lepa1 and lepa2. The strongest stimulatory response was seen for 17 beta-estradiol (E2). E2 treatment significantly up-regulated lepa1 and lepa2 gene expression at doses of 10 nM and 1 nM for each gene, respectively. Lepa1, but not lepa2, was stimulated by T and 11-KT in immature male and immature female parr, while E2 stimulated expression of both genes. The sensitivity to sex steroid stimulation differed in maturing males compared to immature. In maturing males, the androgens and E2 stimulated lepa2 but not lepa1, while in immature males, the androgens and E2 stimulated lepa1, but only E2 stimulated lepa2. The differential response of the two leptin paralogues to the sex steroids suggests differences in regulation of the two leptin genes during maturation. Altogether, these results indicate that leptin expression in Atlantic salmon hepatocytes is directly regulated at the transcriptional level by the main teleost androgens and an estrogen, and that the response might depend on the developmental stage of the fish.

Place, publisher, year, edition, pages
2015. Vol. 221, 156-164 p.
Keyword [en]
Leptin; Sex steroids; Hepatocyte culture; Early sexual maturation; Atlantic salmon; Teleost
National Category
Biological Sciences Developmental Biology
Identifiers
URN: urn:nbn:se:uu:diva-223452DOI: 10.1016/j.ygcen.2015.01.015ISI: 000364983100018PubMedID: 25644210OAI: oai:DiVA.org:uu-223452DiVA: diva2:713103
Funder
Swedish Research Council, 221-2006-1534Swedish Research Council, 229-2010-760
Available from: 2014-04-21 Created: 2014-04-20 Last updated: 2017-12-05Bibliographically approved
In thesis
1. Regulation of Leptin by Sexual Maturation and Energy Status in Male Atlantic Salmon (Salmo salar L.) Parr
Open this publication in new window or tab >>Regulation of Leptin by Sexual Maturation and Energy Status in Male Atlantic Salmon (Salmo salar L.) Parr
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Leptin is a peripheral adiposity signal and a key hormone in energy balance regulation in mammals, acting as a link between nutritional status and the endocrine reproductive axis. If this is also the role of leptin in fish is not fully understood. This thesis investigates how different components of the leptin system are affected by sexual maturation and seasonal changes in energy balance in male Atlantic salmon (Salmo salar L.) parr under fully fed and feed-restricted conditions. Moreover, the role of sex steroids as being one of the possible mechanisms by which sexual maturation interacts with leptin is explored.

The salmon leptin-a genes, lepa1 and lepa2, were expressed mainly in liver and the leptin receptor (lepr) in brain and ubiquitously in peripheral tissues. Seasonal characterization of the lepa genes and lepr during the growth and reproductive season in one-year old males showed that hepatic lepa1 and lepa2 mRNA levels and plasma leptin levels were down-regulated concomitantly with an increase in weight and body fat. Feed restriction up-regulated hepatic leptin, and pituitary lepr expression as well as plasma leptin levels. Correlation between leptin levels and body lipid stores were either lacking or negative. These findings show that leptin and lepr are sensitive to changes in energy balance, but that leptin might not reflect adiposity in juvenile salmon.

Hepatic lepa1 and lepa2, and testicular lepr expression increased during mid- to late spermatogenesis in early maturing males. This up-regulation was preceded by rapid gonadal growth and elevated pituitary follicle-stimulating hormone gene expression levels, whereas peak leptin levels coincided with peak pituitary luteinizing hormone expression and the presence of running milt in the testes. The sex steroids testosterone (T), 11-ketotestosterone and 17-β estradiol stimulated lepa1 and lepa2 gene expression in Atlantic salmon hepatocytes in vitro differentially depending on developmental stage. T was also able to stimulate hepatic lepa1 and pituitary lepa1 and lepr gene expression in immature male salmon in vivo. These results suggest that leptin plays a role in male fish reproduction during later stages of the maturational process and that the elevation of leptin expression during spermatogenesis could be caused by androgen stimulation.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2014. 54 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1151
Keyword
Leptin, leptin receptor, Atlantic salmon, Salmo salar, sexual maturation, puberty, energy balance, hepatocytes, sex steriods
National Category
Biological Sciences
Research subject
Biology with specialization in Comparative Physiology
Identifiers
urn:nbn:se:uu:diva-223462 (URN)978-91-554-8956-4 (ISBN)
Public defence
2014-06-10, Lindahlsalen, Evolutionary Biology Center, Norbyvägen 18A, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2014-05-20 Created: 2014-04-21 Last updated: 2014-06-30

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Trombley, SusanneSchmitz, Monika

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