Direct innervation of white fat and adrenal medullary catecholamines mediate photoperiodic changes in body fat

2001 ◽  
Vol 281 (5) ◽  
pp. R1499-R1505 ◽  
Author(s):  
Gregory E. Demas ◽  
Timothy J. Bartness

Seasonal adjustments in Siberian hamster adiposity are triggered by day length changes [i.e., short “winter-like” days (SDs) elicit body fat decreases vs. long “summer-like” days (LDs)]. These and other white adipose tissue (WAT) mass decreases traditionally have been ascribed to lipolysis triggered by sympathetically mediated, adrenal medullary released epinephrine; however, recent evidence suggests that direct sympathetic innervation of WAT also is important. Therefore, the contributions of WAT sympathetic innervation and adrenal medullary catecholamines to SD-induced decreases in adiposity were tested. Siberian hamsters were surgically bilaterally adrenal demedullated (ADMEDx) or sham ADMEDx, and all had one inguinal WAT (IWAT) pad sympathectomized via locally injected guanethidine, with the contralateral pad serving as a within-animal innervated control. One-half of the hamsters remained in LDs; the remainder was transferred to SDs. Guanethidine and ADMEDx abolished IWAT norepinephrine and adrenal epinephrine contents, respectively. Although sympathetic denervation or ADMEDx alone did not block SD-induced decreases in IWAT mass, their combination did. These results suggest that both adrenal catecholamines and the sympathetic innervation of WAT interact to decrease SD-induced decreased adiposity.

2005 ◽  
Vol 289 (2) ◽  
pp. R514-R520 ◽  
Author(s):  
Haifei Shi ◽  
Timothy J. Bartness

The sensory innervation of white adipose tissue (WAT) is indicated by the labeling of sensory bipolar neurons in the dorsal root ganglion after retrograde dye placement into WAT. In addition, immunoreactivity (ir) for sensory-associated neuropeptides such as calcitonin gene-related peptide (CGRP) and substance P in WAT pads also supports the notion of WAT sensory innervation. The function of this sensory innervation is unknown but could involve conveying the degree of adiposity to the brain. In tests of total body fat regulation, partial surgical lipectomy triggers compensatory increases in the mass of nonexcised WAT, ultimately resulting in restoration of total body fat levels in Siberian hamsters and other animals. The signal that triggers this compensation is unknown but could involve disruption of WAT sensory innervation that accompanies lipectomy. Therefore, a local and selective sensory denervation was accomplished by microinjecting the sensory nerve neurotoxin capsaicin bilaterally into epididymal WAT (EWAT) of Siberian hamsters, whereas controls received vehicle injections. Additional hamsters had bilateral EWAT lipectomy (EWATx) or sham lipectomy. As seen previously, EWATx resulted in significantly increased retroperitoneal WAT (RWAT) and inguinal WAT (IWAT) masses. Capsaicin treatment significantly decreased CGRP- but not tyrosine hydroxylase-ir, attesting to the diminished and selective sensory innervation. Capsaicin-treated hamsters also had increased RWAT and, to a lesser degree, IWAT mass largely mimicking the WAT mass increases seen after lipectomy. Collectively, these data suggest the possibility that information related to peripheral lipid stores may be conveyed to the brain via the sensory innervation of WAT.


2001 ◽  
Vol 60 (3) ◽  
pp. 357-364 ◽  
Author(s):  
D. Vernon Rayner

Sympathetic stimulation has long been recognized to mobilise fatty acids from white adipose tissue. However, it is now apparent that adipose tissue is not only concerned with energy storage as fat, but is a major endocrine and secretory organ. This change has resulted from the identification of leptin as a hormone of energy balance secreted by white adipose tissue. The sympathetic system is a key regulator of leptin production in white fat. Sympathomimetic amines, cold exposure or fasting (which lead to sympathetic stimulation of white fat), decrease ob gene expression in the tissue and leptin production. On the other hand, sympathetic blockade often increases circulating leptin and ob gene expression, and it is postulated that the sympathetic system has a tonic inhibitory action on leptin synthesis. In rodents this action is through stimulation of b3-adrenoceptors. The adrenal medulla (as opposed to the direct sympathetic innervation) has been thought to play only a minor role in the catecholaminergic regulation of white adipose tissue. However, in rodents responses of the leptin system to adrenergic blockade vary with the method used. Changes in leptin and ob gene expression are considerably less using methods of blockade that only effect the terminal adrenergic innervation, rather than medullary secretions as well. Stimulation of the leptin system increases sympathetic activity and hence metabolic activity in many tissues. As well as leptin, other (but not all) secretions from white adipose tissue are subject to sympathetic regulation. In obesity the sympathetic sensitivity of adipose tissue is reduced and this factor may underlie the dysregulation of leptin production and other adipose tissue secretions.


2005 ◽  
Vol 289 (2) ◽  
pp. R380-R388 ◽  
Author(s):  
Eva L. Lacy ◽  
Timothy J. Bartness

Surgical removal of body fat (lipectomy) triggers compensatory increases in nonexcised white adipose tissue (WAT), thus restoring adiposity levels in many species, including Siberian hamsters. In Siberian hamsters, when their lipectomized WAT is transplanted to another site (autologous grafts, no net change in body fat), healthy grafts result, but the lipectomy-induced compensatory increases in nonexcised WAT masses are exaggerated, an effect that apparently occurs only when the grafts contact intact WAT. When WAT is added to nonlipectomized hamsters to increase body fat, native WAT pads do not decrease. Thus WAT addition or removal-replacement does not induce compensatory WAT responses consistent with total body fat regulation as does WAT subtraction. Therefore, we tested whether the exaggerated response to lipectomy occurring with autologous WAT transplantation is dependent on graft site placement and whether the donor graft source [inguinal or epididymal WAT (IWAT, EWAT), sibling vs. nonsibling] affected body fat responses to WAT additions in nonlipectomized hamsters. Lipectomized hamsters received subcutaneous autologous EWAT grafts placed remotely from other WAT (ventrum) or in contact with intact WAT (dorsum), whereas intact hamsters received EWAT or IWAT grafts from sibling or nonsibling donors. The exaggerated response to lipectomy only occurred when grafts were in contact with intact WAT. EWAT, but not IWAT, additions to nonlipectomized siblings or nonsiblings increased native IWAT and retroperitoneal WAT mass but not EWAT mass compared with controls. Collectively, WAT transplantation to either lipectomized or nonlipectomized hamsters increased body fat contingent on graft contact with intact or native WAT.


1996 ◽  
Vol 270 (2) ◽  
pp. R383-R392 ◽  
Author(s):  
M. M. Mauer ◽  
T. J. Bartness

Long day (LD)-housed Siberian hamsters show compensatory mass increases in nonexcised white adipose tissue (WAT) after partial lipectomy, whereas hamsters exposed to short days (SDs) for 22 wk do not. The purpose of this experiment was to determine the cellularity changes underlying lipectomy-induced WAT compensation and whether the duration of SD exposure affects this compensation. Male Siberian hamsters were epididymal (E) or inguinal (I) WAT lipectomized (x) or sham-lipectomized (Sham) and either remained in LDs or were transferred to SDs and killed 6 or 12 wk later. In LDs, lipectomized hamsters showed compensatory mass increases in retroperitoneal WAT (RWAT) due to hyperplasia. IWAT mass also was increased by approximately 40% in LD-housed EWATx hamsters because of nonsignificant increases in adipocyte size and number at weeks 6 and 12, respectively. SD-housed hamsters responded to lipectomy by delaying the SD-associated body fat loss so that RWAT mass was reduced only one-third as much in lipectomized as in Sham hamsters, and the IWAT adipocytes of EWATx hamsters were larger than in Sham hamsters at week 6. At week 12, there was little indication of fat pad compensation by SD-housed hamsters. Collectively, the results of the present experiment and our previous study (16) suggest that the inhibitory effect of SDs on fat pad compensation after lipectomy increases with prolonged SD exposure.


1997 ◽  
Vol 273 (6) ◽  
pp. R2117-R2123 ◽  
Author(s):  
Mary Margaret Mauer ◽  
Timothy J. Bartness

Long day-housed Siberian hamsters show compensatory mass increases in inguinal (I) white adipose tissue (WAT) after epididymal WAT pad (EWAT) removal (x) but do not increase EWAT mass after IWATx. This study tested whether EWAT is specifically unresponsive to IWATx or whether EWAT lacks responsiveness to body fat deficits in general. We also tested whether the compensatory mass increases that occur after side-specific body fat removal are unilateral or bilateral. Therefore EWAT and/or IWAT was removed unilaterally or bilaterally. The compensatory changes in WAT mass by the intact fat pads were measured 12 wk later. EWAT did not compensate for removal of its contralateral mate. Retroperitoneal WAT and IWAT showed greater compensatory mass increases ipsilateral to the side of fat pad removal when EWAT or IWAT pads were removed unilaterally but not after removal of larger amounts of body fat. These results suggest the following: 1) in general, the greater the lipectomy-induced lipid deficit, the greater is the relative fat pad mass compensation; 2) the restoration of body fat content after lipectomy may involve mechanisms that can detect the side of the lipid deficit and enhance fat deposition on this side; and 3) EWAT does not show compensatory mass increases after lipectomy.


Physiology ◽  
2021 ◽  
Vol 36 (4) ◽  
pp. 246-255
Author(s):  
Heike Münzberg ◽  
Elizabeth Floyd ◽  
Ji Suk Chang

Obesity research progresses in understanding neuronal circuits and adipocyte biology to regulate metabolism. However, the interface of neuro-adipocyte interaction is less studied. We summarize the current knowledge of adipose tissue innervation and interaction with adipocytes and emphasize adipocyte transitions from white to brown adipocytes and vice versa. We further highlight emerging concepts for the differential neuronal regulation of brown/beige versus white adipocyte and the interdependence of both for metabolic regulation.


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