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Department of Biology, Neurobiology and Behavior Program and National Science Foundation Center for Behavioral Neuroscience, Georgia State University, Atlanta, Georgia 30303 - 3083
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Many animals show seasonal changes in adiposity that are triggered by changes in the photoperiod. For example, in short "winterlike" days, the nocturnal duration of pineal melatonin (MEL) secretion increases ultimately resulting in body fat decreases by Siberian hamsters. These decreases in body fat are mediated through increases in the sympathetic drive on white adipose tissue (WAT). The central nervous system (CNS) origins of the sympathetic outflow from brain to WAT include the suprachiasmatic nucleus (SCN), an area necessary for the reception of season-encoded MEL signals in Siberian hamsters. Therefore, we tested whether SCN neurons that are part of the sympathetic outflow to WAT also express MEL receptors (MEL1a). This was accomplished by labeling the sympathetic outflow from brain to WAT using a transsynaptic retrograde tract tracer, the pseudorabies virus (PRV), injected into inguinal WAT combined with labeling of brain MEL1a receptors using in situ hybridization. We found PRV-labeled neurons that also expressed MEL1a-receptor mRNA in several brain regions including the SCN. Thus the increased duration of MEL secretion in short days may increase MEL1a-receptor stimulation that, in turn, increases the sympathetic drive on WAT, thereby increasing lipolysis and decreasing adiposity.
adipose tissue; suprachiasmatic nucleus; pseudorabies virus; melatonin 1a receptor; sympathetic nervous system; obesity
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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MANY ANIMALS EXHIBIT SEASONAL responses including changes in reproductive status and behavior (32), body and lipid mass (11, 16, 42), pelage color and thickness (15, 21, 24), immune function (18, 47), and thermoregulation (23, 29; for review, see Refs. 20, 24, 45). For some species, these seasonal responses are triggered by changes in the photoperiod (day length). That is, changes in the photoperiod are faithfully transduced into a biochemical signal via the nocturnal synthesis and secretion of melatonin (MEL) by the pineal gland (for review, Ref. 8). Thus, in short "winterlike" days, the nights are longer than in long "summerlike" days and, therefore, the peak duration of nocturnally secreted MEL is lengthened (25). Siberian hamsters (Phodopus sungorus) exposed to short days decrease their body and lipid mass (24, 38, 42) and show reproductive inhibition (24). These naturally occurring short-day responses can be duplicated in the laboratory by giving pinealectomized Siberian hamsters short day-like MEL signals via timed, subcutaneous MEL infusions (7; for review, see Ref. 10).
The MEL1a receptor is the functional MEL-receptor subtype for photoperiodic responses in Siberian hamsters and many other photoperiodic species (33, 43). Siberian hamsters express brain MEL1a receptors predominantly in the paraventricular (PVT) and reuniens (ReN) nuclei of the thalamus and in the suprachiasmatic nucleus of the hypothalamus (SCN) (19, 37, 44). Of these areas, the SCN appears critical in the reception of season-encoded MEL signals, because pinealectomized Siberian hamsters bearing SCN lesions do not exhibit short day-like responses when given exogenously administered short day MEL signals including the decrease in adiposity (9, 35, 36).
One possible mechanism underlying the short day-induced decreases in body fat may involve the sympathetic nervous system mobilization of lipid from white adipose tissue (WAT). That is, short days increase the sympathetic drive (e.g., increase norepinephrine turnover) on WAT (48); accordingly, the greater the short-day-induced increase in norepinephrine turnover in WAT depots, the greater the degree of lipid mobilization (48).
The origins of the sympathetic outflow from brain to WAT have been defined using the transneuronal retrograde viral tract tracer, the pseudorabies virus [PRV (2)]. Injections of PRV into WAT pads result in labeling of a hierarchical chain of functionally connected neurons that include all levels of the neuroaxis. Because MEL1a receptors are expressed in brain areas that also are part of the sympathetic outflow from brain to WAT (2), including the SCN (33, 43), we reasoned that the short day-like MEL signals might stimulate these central nervous system (CNS) sympathetic outflow neurons that ultimately project to WAT. This, in turn, may lead to increases in the sympathetic drive on white adipocytes, thereby increasing lipolysis and decreasing adiposity. Therefore, the purpose of this study was to determine whether the SCN neurons that are part of the sympathetic outflow from brain to WAT also express MEL1a receptors.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals. Adult male Siberian hamsters (n = 8) were single-housed in long days (16:8-h light-dark cycle; lights on 0400) and fed Purina rodent chow (#5001; 3.4 kcal/g) and water ad libitum. The animals were derived from our breeding colony established originally from a stock provided by Dr. Bruce Goldman (Univ. of Connecticut) and interbred subsequently with hamsters from Drs. Katherine Wynne-Edwards (Queen's Univ.) and G. Robert Lynch (Univ. of Colorado).
Surgical procedures. Animals were anesthetized with pentobarbital sodium (50 mg/kg), shaved around the hindquarters on the right side, and the shaved area was wiped with ethanol (50%). An incision was made to expose the entire dorsal surface of the inguinal WAT (IWAT) pad, extending from a point near the tail and continuing rostrally along the dorsum adjacent to the spinal column and then caudally close to the ventral midline. Care was taken to avoid damaging the underlying vasculature and musculature. A series of injections of an attenuated strain of the PRV (Bartha's K strain; 1 × 108 plaque-forming U/ml; 150 nl/injection; 5 injections/fat pad; total of 7.5 × 104 plaque-forming units) was made using a microsyringe. The postinjection interval necessary for viral infections in the rostral forebrain when PRV is injected into the IWAT was determined previously to be approximately 6 days (2).
Histology.
Six days postinjection, the animals were perfused transcardially with
heparinized (0.02%) saline and then with the fixative (4%
paraformaldehyde; 0.1 M sodium phosphate buffer; pH 7.4). Brains were
dissected and postfixed in the fixative overnight at 4°C, sunk in a
sucrose solution (30%; with 0.1% sodium azide), and then sliced on a
cryostat (
20°C; 28-µm thickness). Every other section was
processed as follows: sections were immersed in cryoprotectant and
stored in 20°C until processed for combined in situ hybridization
and immunocytochemistry (ICC) for MEL1a receptors and the
virus, respectively, according to our previously published method
(37). The spinal cords also were dissected, postfixed,
sunk in the sucrose solution, embedded in gelatin (20%), sliced to
50-µm thickness along the horizontal plane, and processed for ICC to
visualize PRV.
ICC. The sections were incubated sequentially in the primary antibody (pig polyclonal antibody against PRV; 1:10,000) overnight at 23°C, in secondary antibody (goat antibody against swine; 1:175; Vector Laboratories) for 2 h at 23°C, and then in avidin biotin solution for 1 h at 23°C. The specific labels were detected using diaminobenzidine (0.2 mg/ml; Sigma Chemicals) in the presence of peroxide (0.0025%) as the chromagen.
In situ hybridization/ICC. Briefly, sections were rinsed with 2× saline citrate (SSC; 1× = 0.15 M NaCl; 0.015 M citrate), deaminated in acetic anhydride (0.25%)-triethanolamine (0.1 M in 0.9% NaCl), incubated in formamide (50%; with 2× SSC, 0.1% sodium dodecyl sulfate, 25 mM dithiothreitol), and then hybridized with 35S-labeled MEL1a-receptor cRNA or sense control probes (30,000 cpm/µl) at 57°C overnight. The following day, sections were cooled to room temperature and rinsed sequentially in 1× SSC, 2× SSC-formamide (1:1; 30 min at 53°C), RNAse A (100 mg/ml), 2× SSC-formamide (1:1; 90 min at 53°C), and then in 1× SSC until the sections were processed for ICC to detect PRV, as described above.
Sections were mounted onto gelatin-coated slides, rinsed in deionized water and ethanol (95%), and air-dried. Isotopic labels were detected autoradiographically by dipping sections into NTB3 liquid emulsion (Eastman Kodak, Rochester, NY). Slides were exposed for 16 wk at 4°C, developed and fixed in D-19 and Fixer (Eastman Kodak), counterstained with cresyl violet, and placed on a coverslip. All of the processed brain sections were analyzed for each single label and for double labeling using light microscopy for all nuclei. PRV-infected neurons were considered double labeled if the granular deposition (silver grains) over these cells were at least quadruple that of background levels and conformed to the shape of the cell bodies, as we have done previously (37).Statistical analysis. All measures were analyzed using a one-way analysis of variance for related samples (SigmaStat; v2.03) and post hoc comparisons between measures made using Duncan's New Multiple Range Test (26). All differences were considered statistically significant at P < 0.05. Test values and exact probabilities are not presented for clarity and simplicity of presentation.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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PRV infection.
There were no signs of sickness in the animals after PRV injections. In
addition, histological examination of the spinal cord indicated PRV
infection ipsilateral but not contralateral to the injection site (Fig.
1). This unilateral PRV infection pattern in the spinal cord and the lack of illness in the animals indicated that this virus titer produced a controlled and specific viremia. PRV-immunoreactive neurons in the forebrain were found in the SCN,
retrochiasmatic area, periventricular area (PeVN), paraventricular hypothalamus (PVN), zona incerta (ZI), ReN/xiphoid nucleus (Xi), anterior hypothalamus (AH), lateral hypothalamus (LH), ventromedial nucleus, dorsomedial nucleus, PVT, perifornical area, arcuate nucleus
(Arc), and the periventricular fiber system.
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MEL1a-receptor expression.
There were MEL1a-receptor mRNA-labeled cells in the SCN
(Fig. 2), PeVN, PVN, ZI, ReN/Xi, AH,
dorsal medial nucleus (DMN), PVT, perifornical area, periventricular
fiber system, and, most impressively, in the pars tuberalis (PT; Fig.
3). Hybridization with sense control
probes caused no specific labeling.
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PRV-infected cells that expressed MEL1a receptors.
There were PRV immunoreactive cells that also were labeled for
MEL1a-receptor mRNA (MEL1a + PRV) in the
SCN (Fig. 4), PeVN (Fig. 5), PVN, ZI (Fig. 6), ReN/Xi,
AH, DMN (Fig. 7), PVT, perifornical area,
and periventricular fiber system.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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In the present study, we found that some of the SCN neurons that were part of the sympathetic outflow from brain to WAT expressed MEL1a-receptor mRNA. This finding lends support for the notion that season-encoded MEL signals stimulate this population of MEL1a receptors to increase the sympathetic drive on WAT, ultimately triggering the short-day-induced increases in lipid mobilization (i.e., increases in lipolysis) and the consequent decreases in body fat by Siberian hamsters.
The SCN contained the highest number of MEL1a + PRV neurons compared with the other brain areas exhibiting MEL1a gene expression; however, there were also substantial numbers of MEL1a + PRV colocalized cells in the PVN, ZI, ReN/XI, and DMN and, to a lesser degree, in the PeVN, PVT, AH, perifornical area, and periventricular fiber system. The degree of MEL1a + PRV colocalization, if compared as percentages of the total number of PRV-infected neurons within the individual structures, is most prominent in the PVT followed by the SCN and then in descending order by ReN/Xi, DMN, periventricular fiber system, ZI, perifornical area, PVN, PeVN, and AH (Fig. 8B).
As suggested above, the relative overlap of the distribution of PRV-infected neurons with MEL1a-receptor mRNA expression was considerable and especially prominent in the SCN and PVT. Although no evidence suggests involvement of the PVT in lipid mobilization, whether photoperiod-induced or induced by other means (e.g., fasting or cold exposure), the PVT projects to areas that are part of the sympathetic outflow to WAT, areas that have been implicated in the regulation of body fat [e.g., SCN, DMN, and amygdala (30; for review, see Refs. 4, 5)].
In contrast to the PVT, the SCN has been shown to be involved in increased lipid mobilization generally (22, 41, 46; for review, see Ref. 5) and in increased photoperiod-induced lipid mobilization specifically (9, 35, 36). For example, coronal microknife cuts just behind the SCN block increases in lipid mobilization associated with 24-h fasts, forced exercise (swimming), cold exposure, and insulin-induced hypoglycemia in rats (14). Furthermore, microinfusions of short day-like MEL signals into the SCN trigger short day-like responses in Siberian hamsters (1), including decreases in body fat (T. G. Youngstrom and T. J. Bartness, unpublished data). Moreover, SCN lesions block the ability of short-day-like exogenous MEL signals to decrease body and fat pad masses in pinealectomized Siberian hamsters (5, 9, 35, 36).
We expected a higher degree of MEL1a + PRV colocalization dorsomedially than ventrolaterally within the SCN, because PRV injected into IWAT concentrates in the dorsomedial SCN where MEL1a receptors are more dense (Fig. 4) (28, 37). We found, however, that MEL1a + PRV cells were distributed evenly between these two SCN subregions (data not shown). Although a complete description of the topography of SCN efferent projections is unknown presently, the most detailed work to date describes the innervation of the rat pineal gland (27). Here SCN efferents involved in the sympathetic outflow to the pineal gland originate in dorsal, medial, and ventral areas (27). Moreover, these neurons may also be part of a general sympathetic outflow to multiple peripheral targets (39) including WAT.
Although we focused on the sympathetic outflow from brain to WAT as the primary means for short-day-induced decreases in body mass in the present study, surgical (49) or chemical sympathetic denervation of WAT only partially blocks short-day-induced body fat decreases (G. E. Demas and T. J. Bartness, unpublished data). Similarly, removal of the other branch of the sympathetic outflow, the adrenal medulla (adrenal demedullation), and, consequently, the abolition of epinephrine-induced lipolysis, only partially block short-day-induced body fat decreases (G. E. Demas and T. J. Bartness, unpublished data). Sympathetic denervation of WAT combined with adrenal demedullation, however, completely block short day-induced body fat decreases (G. E. Demas and T. J. Bartness, unpublished data). Perhaps the ability of SCN lesions to completely block short-day-induced lipid mobilization by Siberian hamsters is due to a centrally induced blockade of sympathetic outflow to both the adrenal medulla and WAT. It is unknown whether there are MEL receptors on neurons comprising the brain-sympathetic nervous system-adrenal medulla circuitry; however, the patterns of infection after PRV injections into rat (40) or Siberian hamster (G. E. Demas and T. J. Bartness, unpublished data) adrenal medulla vs. WAT (2, 34) are quite similar.
Finally, we found MEL1a-receptor mRNA expressed in the SCN, AH, PVT, DMN, ReN/Xi, PeVN, perifornical area, periventricular fiber system, and PT, as indicated above. This is consistent with our previous findings (37) with one minor difference. In the present experiment, we also found MEL1a-receptor mRNA-positive cells in the PVN and ZI. Neurons in these two areas were few in number and may be cells located slightly peripherally to the distribution of MEL1a receptors that encompasses the PVT/ReN/Xi area. The longer emulsion-exposure time used in the present study (16 wk) compared with our previous studies [12 wk (37)] likely enhanced autoradiographic labeling, including that seen in the PVN and ZI.
In summary, our findings provide neuroanatomic evidence that suggests the following possible scenario: 1) short days increase the duration of nocturnal MEL secretion, 2) increases in the duration of nocturnal MEL increase stimulation of MEL1a receptors in several forebrain areas (e.g., SCN) that are part of the sympathetic outflow to WAT, 3) stimulation of these MEL1a receptors may increase the sympathetic drive on WAT, 4) increases in sympathetic drive on WAT increase lipolysis, and 5) increases in lipolysis lead to the characteristic short-day-induced decrease in adiposity in Siberian hamsters.
Perspectives
Environmental influences are recognized as important factors contributing to the etiology of human obesity (e.g., see Ref. 31). Although this point might seem obvious, the role of the environment in energy regulation is underrepresented in animal models of human energy balance disorders where emphasis is mostly on genetic factors (e.g., see Ref. 13). Because reversibility of the obesity exhibited by many genetic and brain-lesion models is difficult or impossible, our understanding of body fat decreases, especially naturally occurring body fat decreases, lags far behind our understanding of factors promoting body fat increases. To our knowledge, the present data are the only example where the influence of a critical environmental factor affecting adiposity can be traced from the reception of that stimulus to the ultimate changes in fat cell size. Specifically, for photoperiod-induced body fat decreases in Siberian hamsters, we know 1) the critical environmental stimulus (i.e., the photoperiod; for review see, Refs. 6, 12), 2) its transduction into a biochemical signal [i.e., the pineal via changes in the durational secretion of MEL (8, 10)], 3) the reception of this signal [i.e., MEL1a receptors (33, 37) located on neurons comprising the origins of sympathetic outflow], 4) the transmission of this signal to the adipocytes (i.e., via the sympathetic innervation of WAT), 5) the mechanism by which lipid is mobilized [i.e., increased sympathetic drive (48)], and 6) the adipose tissue cellularity response [i.e., decreased fat cell size (3)]. Although the relevance of photoperiod/MEL-induced changes in body fat for human obesity is unknown, this model of naturally occurring changes in body fat may prove useful in understanding how these and other animals in the wild shift from obese to less obese states, seemingly with relative ease.| |
ACKNOWLEDGEMENTS |
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We thank Drs. D. Weaver and S. Reppert for the MEL1a-receptor cDNA (Genbank Accession #U14110) and Dr. K. Platt for the pig polyclonal antibody against PRV. We also thank Drs. L. Lubbers and S. Petersen for technical advice and A. Harris and Dr. L. Ganaway for technical assistance.
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FOOTNOTES |
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This research was supported by National Institutes of Health research Grant RO1 DK-35254 and National Institute of Mental Health research scientist development award KO2 MH-00841 and Georgia State University Research Enhancement Fund to T. J. Bartness.
Address for reprint requests and other correspondence: T. J. Bartness, Dept. of Biology, 24 Peachtree Center Ave. NE, Georgia State Univ., Atlanta, GA 30303-3083 (E-mail: bartness{at}gsu.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 25 January 2001; accepted in final form 17 April 2001.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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