An intact dorsomedial hypothalamic nucleus, but not the subzona incerta or reuniens nucleus, is necessary for short-day melatonin signal-induced responses in Siberian hamsters - PubMed (original) (raw)
An intact dorsomedial hypothalamic nucleus, but not the subzona incerta or reuniens nucleus, is necessary for short-day melatonin signal-induced responses in Siberian hamsters
Claudia Leitner et al. Neuroendocrinology. 2011.
Abstract
Siberian hamsters provide a useful model to define mechanisms underlying obesity reversal as they naturally transition from their extreme seasonal obesity in long 'summer-like' days (LDs) to a leaner state in short 'winter-like' days (SDs). These day length changes are coded into durational melatonin (MEL) signals by the pineal gland resulting in stimulation of MEL receptors (MEL(1a)-Rs). MEL(1a)-R mRNA is colocalized centrally in sympathetic nervous system (SNS) outflow neurons comprising a chain of neurons that ultimately innervates white adipose tissue (WAT). Neural components in this circuit include the subzona incerta (subZI), dorsomedial hypothalamic nucleus (DMH) and thalamic reuniens nucleus (ReN). SD, long-duration MEL signals induce gonadal regression and increase WAT SNS drive triggering lipolysis and thereby reversing LD obesity. We attempted to block the reversal of SD MEL signal-induced obesity by making electrolytic or sham lesions of the subZI, ReN or DMH in LD-housed hamsters. To create SD-like, long-duration MEL signals, we injected MEL 3 h before lights out, thereby lengthening the naturally occurring nocturnal duration of circulating MEL. ReN and subZI lesions did not block SD-like MEL signal-induced decreases in body, WAT, testicular masses or food intake; by contrast, DMH lesions blocked decreases in WAT and testicular mass. This nonresponsiveness was not due to lesion-induced inappropriate nocturnal LD MEL secretion that would have altered our creation of SD-like signals. Therefore, the DMH appears to participate in the control of both SD energy and reproductive responses, and joins the suprachiasmatic nucleus as sites necessary for SD responses in this species.
Copyright © 2010 S. Karger AG, Basel.
Figures
Fig. 1
Lesion verification. Photographic representation of lesion of the ReN, subZI and DMH in Siberian hamsters exposed to SD-like MEL signals for 5 weeks.
Fig. 2
Testicular response. a Mean ± SEM percent change from control (saline-treated, sham-operated) of testes mass (g) in MEL-treated Siberian hamsters bearing lesions at the ReN, subZI and DMH. b Mean ± SEM percent change from control (saline-treated, sham-operated) of serum testosterone levels (ng/ml) in MEL-treated Siberian hamsters bearing lesions of the ReN, subZI and DMH. a p < 0.05 between saline and MEL treatment; b p < 0.05 between MEL/lesion and all other groups. Number of animals: saline/sham, saline/lesion, MEL/sham, MEL/lesion, respectively: ReN n = 9, 10, 10, 7; subZI n = 9, 7, 10, 7; DMHx n = 7, 5, 11, 7.
Fig. 2
Testicular response. a Mean ± SEM percent change from control (saline-treated, sham-operated) of testes mass (g) in MEL-treated Siberian hamsters bearing lesions at the ReN, subZI and DMH. b Mean ± SEM percent change from control (saline-treated, sham-operated) of serum testosterone levels (ng/ml) in MEL-treated Siberian hamsters bearing lesions of the ReN, subZI and DMH. a p < 0.05 between saline and MEL treatment; b p < 0.05 between MEL/lesion and all other groups. Number of animals: saline/sham, saline/lesion, MEL/sham, MEL/lesion, respectively: ReN n = 9, 10, 10, 7; subZI n = 9, 7, 10, 7; DMHx n = 7, 5, 11, 7.
Fig. 3
Changes in body mass (a) and food intake (b). a Mean ± SEM percent change of body mass after 5 weeks of MEL treatment in Siberian hamsters bearing lesions of the ReN, subZI and DMH or sham-operated animals. b Mean ± SEM percent change of food intake after 5 weeks of MEL treatment in Siberian hamsters bearing lesions of the ReN, subZI and DMH or sham-operated animals. a p < 0.05 between saline and MEL treatment. Number of animals: saline/sham, saline/lesion, MEL/sham, MEL/lesion, respectively: ReN n = 9, 10, 10, 7; subZI n = 9, 7, 10, 7; DMHx n = 7, 5, 11, 7.
Fig. 3
Changes in body mass (a) and food intake (b). a Mean ± SEM percent change of body mass after 5 weeks of MEL treatment in Siberian hamsters bearing lesions of the ReN, subZI and DMH or sham-operated animals. b Mean ± SEM percent change of food intake after 5 weeks of MEL treatment in Siberian hamsters bearing lesions of the ReN, subZI and DMH or sham-operated animals. a p < 0.05 between saline and MEL treatment. Number of animals: saline/sham, saline/lesion, MEL/sham, MEL/lesion, respectively: ReN n = 9, 10, 10, 7; subZI n = 9, 7, 10, 7; DMHx n = 7, 5, 11, 7.
Fig. 4
Decrease in total dissected WAT. Mean ± SEM percent change from controls (saline-treated, sham-operated) of fat pad mass (g) in Siberian hamsters bearing lesions of the ReN, subZI, and DMH. a p < 0.05 between saline and MEL treatment; b p < 0.05 between sham-operated animals and animals bearing lesions. Number of animals: saline/sham, saline/lesion, MEL/sham, MEL/lesion, respectively: ReN n = 9, 10, 10, 7; subZI n = 9, 7, 10, 7; DMHx n = 7, 5, 11, 7.
Fig. 5
Nocturnal MEL secretion in Siberian hamsters with DMHx. Mean ± SEM percent change of MEL concentrations (pg/ml) of Siberian hamsters with DMHx and sham-operated animals. The thick black bar represents the duration of the dark period vs. the thin bar, which represents the light phase. * p < 0.05 from baseline (–2 h). Number of animals: DMHx n = 8, sham n = 5.
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References
- Flegal KM. Epidemiologic aspects of overweight and obesity in the United States. Physiol Behav. 2005;86:599–602. - PubMed
- Satcher D: Overweight and obesity threaten U.S. health gains. www.surgeongeneral.gov/topics/obesity
- Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA. 2006;295:1549–1555. - PubMed
- Bartness TJ, Wade GN. Photoperiodic control of seasonal body weight cycles in hamsters. Neurosci Biobehav Rev. 1985;9:599–612. - PubMed
- Mercer JG. Regulation of appetite and body weight in seasonal mammals. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol. 1998;119:295–303. - PubMed
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