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Regulation of Leptin by Sexual Maturation and Energy Status in Male Atlantic Salmon (Salmo salar L.) Parr
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Comparative Physiology.
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 [en]
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: urn:nbn:se:uu:diva-223462ISBN: 978-91-554-8956-4 (print)OAI: oai:DiVA.org:uu-223462DiVA: diva2:713160
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
List of papers
1. Effects of long-term restricted feeding on plasma leptin, hepatic leptin expression and leptin receptor expression in juvenile Atlantic salmon (Salmo salar L.)
Open this publication in new window or tab >>Effects of long-term restricted feeding on plasma leptin, hepatic leptin expression and leptin receptor expression in juvenile Atlantic salmon (Salmo salar L.)
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2012 (English)In: General and Comparative Endocrinology, ISSN 0016-6480, E-ISSN 1095-6840, Vol. 175, no 1, 92-99 p.Article in journal (Refereed) Published
Abstract [en]

Leptin is a pleiotropic hormone and plays a key role in body weight regulation, energy homeostasis and lipid store utilization in mammals. In this study, we investigated the effect of feed-restriction on leptin genes (lepa1 and lepa2), leptin receptor (lepr) gene expression and plasma leptin levels in juvenile Atlantic salmon parr. Feed restriction was performed from late April to mid-June, in order to gain insight into the role of the leptin system in energy balance regulation and adiposity in juvenile salmon. A significant increase in lepa1 expression as well as higher levels of plasma leptin was found in feed-restricted fish in June compared to fully fed controls, while lepa2 gene expression decreased in both groups during the treatment period. Lepa2 was, however significantly higher in the feed-restricted group in June. Leptin receptor expression was up regulated during the period of enhanced growth and lipid deposition in the fully fed control, indicating a seasonal effect on the receptor expression in the brain. Both lepa1 and lepa2 genes very mainly expressed in the liver in juvenile salmon, while lepr was expressed in the brain but showed also considerable expression in various peripheral tissues. The study provides evidence that the leptin system is sensitive to the metabolic status of the fish as both season and restricted feeding affect lepa1 and lepa2 gene expression in the liver and brain leptin receptor expression, however, for lepa1 expression and leptin plasma level in an opposite way as that observed in the mammalian system.

National Category
Zoology
Research subject
Biology with specialization in Comparative Physiology
Identifiers
urn:nbn:se:uu:diva-166581 (URN)10.1016/j.ygcen.2011.10.001 (DOI)000299065800012 ()22019478 (PubMedID)
Funder
Formas, 2010-03-11
Available from: 2012-01-12 Created: 2012-01-12 Last updated: 2017-12-08Bibliographically approved
2. Regulation of the seasonal leptin and leptin receptor expression profile during early sexual maturation and feed restriction in male Atlantic salmon, Salmo salar L., parr
Open this publication in new window or tab >>Regulation of the seasonal leptin and leptin receptor expression profile during early sexual maturation and feed restriction in male Atlantic salmon, Salmo salar L., parr
2014 (English)In: General and Comparative Endocrinology, ISSN 0016-6480, E-ISSN 1095-6840, Vol. 204, 60-70 p.Article in journal (Refereed) Published
Abstract [en]

In mammals, leptin acts as an adiposity signal and is a crucial link between nutritional status and the reproductive axis. So far the link between leptin and energy balance during sexual maturation in teleosts has been poorly investigated. In this study, seasonal gene expression changes in two leptin genes (lepa1 andlepa2) and the leptin receptor were investigated during early sexual maturation in male Atlantic salmon parr under fully fed (control) and feed restricted conditions from April through September. Both Atlantic salmonlepa1 and lepa2 in the liver and lepr in the brain were significantly down-regulated in non-maturing control males in early spring, coinciding with the start of the growth and fat accumulation. In maturing control males, hepatic leptin expression increased during mid-spermatogenesis and lepa1 and lepa2 mRNA levels were up-regulated by 7.7 and 49 times respectively during final maturation. For the first time in a fish species, a significant up-regulation of lepr expression was observed in the testis throughout mid to late spermatogenesis. Feed restriction decreased the incidence of sexual maturation by 53% and highly up-regulated both leptin genes in the liver and the leptin receptor in the pituitary. This study shows that hepaticlepa1 and lepa2 expression and lepr expression in the testis is affected by early sexual maturation in male Atlantic salmon parr. Fast growth and high fat stores are associated with low leptin levels while feed restriction has a stimulatory effect on hepatic leptin and leptin receptor gene expression in the pituitary, suggesting a role for leptin other than that as an adiposity signal.

Keyword
Leptin, leptin receptor, sexual maturation, restricted feeding, Atlantic salmon, teleost
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-223453 (URN)10.1016/j.ygcen.2014.04.033 (DOI)000341616200008 ()
Available from: 2014-04-21 Created: 2014-04-20 Last updated: 2017-12-05Bibliographically approved
3. Sex steroids stimulate leptin gene expression in Atlantic salmon parr hepatocytes in vitro
Open this publication in new window or tab >>Sex steroids stimulate leptin gene expression in Atlantic salmon parr hepatocytes in vitro
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.

Keyword
Leptin; Sex steroids; Hepatocyte culture; Early sexual maturation; Atlantic salmon; Teleost
National Category
Biological Sciences Developmental Biology
Identifiers
urn:nbn:se:uu:diva-223452 (URN)10.1016/j.ygcen.2015.01.015 (DOI)000364983100018 ()25644210 (PubMedID)
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
4. Effects of testosterone and 11-ketoandrostenedione on leptin and the leptin receptor in immature male Atlantic salmon, Salmo salar L., parr
Open this publication in new window or tab >>Effects of testosterone and 11-ketoandrostenedione on leptin and the leptin receptor in immature male Atlantic salmon, Salmo salar L., parr
(English)Manuscript (preprint) (Other academic)
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-223454 (URN)
Available from: 2014-04-21 Created: 2014-04-20 Last updated: 2014-06-30

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