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Photoperiod-induced increases in bone mineral apposition rate in Siberian hamsters and the involvement of seasonal leptin changes

Kokolski, Marie; Ebling, Francis J.; Henstock, James R.; Anderson, Susan I.

Photoperiod-induced increases in bone mineral apposition rate in Siberian hamsters and the involvement of seasonal leptin changes Thumbnail


Authors

Francis J. Ebling

James R. Henstock

Susan I. Anderson



Abstract

The adipokine leptin regulates energy balance, appetite, and reproductive maturation. Leptin also acts on bone growth and remodeling, but both osteogenic and anti-osteogenic effects have been reported depending on experimental conditions. Siberian hamsters (Phodopus sungorus) have natural variation in circulating leptin concentrations, where serum leptin is significantly decreased during the short day (SD)-induced winter state. In summer long day (LD) photoperiods, appetite and body adiposity increase with associated central leptin insensitivity. This natural change in leptin secretion was exploited to investigate leptin’s effect on bone growth. Hamsters were injected with calcium-chelating fluorescent dyes to measure bone mineral apposition rate (MAR). Measurements were initially obtained from 5-week and 6-month-old animals maintained in low leptin (SD) or high leptin (LD) states. A further study investigated effects of chronic administration of recombinant mouse leptin to hamsters housed in SD and LD conditions; growth plate thickness and bone density were also assessed. As expected, a reduction in body mass was seen in hamsters exposed to SD, confirming the phenotype change in all studies. Serum leptin concentrations were significantly reduced in SD animals in all studies. MAR was reproducibly and significantly increased in the femurs of SD animals in all studies. Vitamin D and growth plate thickness were significantly increased in SD animals at 6 months. No effect on bone density was observed in any study. Taken together these data suggest that bone growth is associated with the low leptin, winter, lean state. In leptin-treated animals, there was a significant interaction effect of leptin and photoperiod. In comparison to their vehicle counterparts, SD animals had decreased and LD animals had increased MAR, which was not apparent prior to leptin administration. In conclusion, increased MAR was associated with low serum leptin levels in early life and sustained over 6 months, implying that leptin has a negative effect on bone growth in this model. The unexpected finding that MAR increased after peripheral leptin administration in LD suggests that leptin exerts different effects on bone growth dependent on initial leptin status. This adds further weight to the hypothesis that leptin-treated LD animals display central leptin resistance.

Citation

Kokolski, M., Ebling, F. J., Henstock, J. R., & Anderson, S. I. (2017). Photoperiod-induced increases in bone mineral apposition rate in Siberian hamsters and the involvement of seasonal leptin changes. Frontiers in Endocrinology, 8, Article 357. https://doi.org/10.3389/fendo.2017.00357

Journal Article Type Article
Acceptance Date Dec 7, 2017
Publication Date Jan 1, 2017
Deposit Date Mar 20, 2018
Publicly Available Date Mar 28, 2024
Journal Frontiers in Endocrinology
Electronic ISSN 1664-2392
Publisher Frontiers Media
Peer Reviewed Peer Reviewed
Volume 8
Article Number 357
DOI https://doi.org/10.3389/fendo.2017.00357
Public URL https://nottingham-repository.worktribe.com/output/971276
Publisher URL https://www.frontiersin.org/articles/10.3389/fendo.2017.00357/full

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