White adipose tissue sensory nerve denervation mimics lipectomy-induced compensatory increases in adiposity

2005 ◽  
Vol 289 (2) ◽  
pp. R514-R520 ◽  
Author(s):  
Haifei Shi ◽  
Timothy J. Bartness
Keyword(s):  
Adipose Tissue ◽  
Body Fat ◽  
White Adipose Tissue ◽  
Sensory Nerve ◽  
Sensory Innervation ◽  
Siberian Hamsters ◽  
Total Body Fat ◽  
Total Body ◽  
Lipid Stores ◽  
The Brain

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.

Innervation of mammalian white adipose tissue: implications for the regulation of total body fat

1998 ◽  
Vol 275 (5) ◽  
pp. R1399-R1411 ◽  
Author(s):  
Timothy J. Bartness ◽  
Maryam Bamshad
Keyword(s):  
Nervous System ◽  
Adipose Tissue ◽  
Body Fat ◽  
White Adipose Tissue ◽  
Regional Differences ◽  
Sensory Innervation ◽  
Exact Nature ◽  
Total Body Fat ◽  
The Central Nervous System ◽  
Total Body

We review the extensive physiological and neuroanatomical evidence for the innervation of white adipose tissue (WAT) by the sympathetic nervous system (SNS) as well as what is known about the sensory innervation of this tissue. The SNS innervation of WAT appears to be a part of the general SNS outflow from the central nervous system, consisting of structures and connections throughout the neural axis. The innervation of WAT by the SNS could play a role in the regulation of total body fat in general, most likely plays an important role in regional differences in lipid mobilization specifically, and may have a trophic affect on WAT. The exact nature of the SNS innervation of WAT is not known but it may involve contact with adipocytes and/or their associated vasculature. We hypothesize that the SNS innervation of WAT is an important contributor to the apparent “regulation” of total body fat.

Effects of white adipose tissue grafts on total body fat and cellularity are dependent on graft type and location

2005 ◽  
Vol 289 (2) ◽  
pp. R380-R388 ◽  
Author(s):  
Eva L. Lacy ◽  
Timothy J. Bartness
Keyword(s):  
Adipose Tissue ◽  
Body Fat ◽  
White Adipose Tissue ◽  
Surgical Removal ◽  
Siberian Hamsters ◽  
Total Body Fat ◽  
Donor Graft ◽  
Total Body ◽  
Tissue Grafts ◽  
Autologous Grafts

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.

Sensory innervation of white adipose tissue

1987 ◽  
Vol 253 (6) ◽  
pp. R942-R944 ◽  
Author(s):  
R. B. Fishman ◽  
J. Dark
Keyword(s):  
Adipose Tissue ◽  
White Adipose Tissue ◽  
Dorsal Root ◽  
Subcutaneous Fat ◽  
Sensory Information ◽  
Sensory Innervation ◽  
Fluorescent Cell ◽  
Fat Depots ◽  
Total Body Fat ◽  
Total Body

The presumption that sensory information does not arise from white adipose tissue was reevaluated using the neuroanatomical tracer, "true blue." Fluorescent cell bodies were observed in dorsal root ganglia of rats after tracer was implanted into inguinal or dorsal subcutaneous fat depots. Sensory information from adipose tissue may play an important role in the regulation of regional and total body fat mass.

Autologous fat transplants influence compensatory white adipose tissue mass increases after lipectomy

2004 ◽  
Vol 286 (1) ◽  
pp. R61-R70 ◽  
Author(s):  
Eva L. Lacy ◽  
Timothy J. Bartness
Keyword(s):  
Adipose Tissue ◽  
Body Fat ◽  
White Adipose Tissue ◽  
Regulatory System ◽  
Ground Squirrels ◽  
Tissue Mass ◽  
Laboratory Rats ◽  
Total Body Fat ◽  
Total Body ◽  
Rats And Mice

Direct tests of the hypothesized total body fat regulatory system have been accomplished by partial surgical lipectomy. This usually results in the restoration of the lipid deficit through compensatory increases in nonexcised white adipose tissue (WAT) masses of ground squirrels, laboratory rats, and mice, as well as Siberian and Syrian hamsters. We challenged this hypothesized total body fat regulatory system by testing the response of Siberian hamsters to 1) lipid deficits [lipectomy; primarily bilateral epididymal WAT (EWAT) removal], 2) lipid surfeits (addition of donor EWAT with no lipectomy), 3) no net change in lipid [EWAT or inguinal WAT (IWAT) lipectomy with the excised fat replaced to a new location (autologous)], 4) lipectomy with the same pad (EWAT lipectomy only) added from a sibling (nonautologous), and 5) sham surgeries for each treatment. Food intake generally was not affected. Body mass was not affected across all treatments. Grafts ∼3 mo later had normal appearance both macro- and microscopically and were revascularized. The normal lipectomy-induced compensatory increases in nonexcised WAT masses surprisingly were exaggerated with autologous EWAT transplants, but not for autologous IWAT or nonautologous EWAT transplants. There was no compensatory decrease in native WAT masses with nonautologous EWAT additions. Collectively, only lipectomy triggered reparation of the lipid deficit, but the other manipulations did not, suggesting a system biased toward rectifying decreases in lipid or an inability of the hypothesized total body fat regulatory system to recognize WAT transplants.

scholarly journals Brain–adipose tissue cross talk

2005 ◽  
Vol 64 (1) ◽  
pp. 53-64 ◽  
Author(s):  
Timothy J. Bartness ◽  
C. Kay Song ◽  
Haifei Shi ◽  
Robert R. Bowers ◽  
Michelle T. Foster
Keyword(s):  
Nervous System ◽  
Adipose Tissue ◽  
Body Fat ◽  
Pseudorabies Virus ◽  
Sensory Nerve ◽  
Sensory Innervation ◽  
Electrophysiological Recording ◽  
Surgical Removal ◽  
Fat Cell ◽  
The Brain

While investigating the reversible seasonal obesity of Siberian hamsters, direct sympathetic nervous system (SNS) postganglionic innervation of white adipose tissue (WAT) has been demonstrated using anterograde and retrograde tract tracers. The primary function of this innervation is lipid mobilization. The brain SNS outflow to WAT has been defined using the pseudorabies virus (PRV), a retrograde transneuronal tract tracer. These PRV-labelled SNS outflow neurons are extensively co-localized with melanocortin-4 receptor mRNA, which, combined with functional data, suggests their involvement in lipolysis. The SNS innervation of WAT also regulates fat cell number, as noradrenaline inhibits and WAT denervation stimulates fat cell proliferation in vitro and in vivo respectively. The sensory innervation of WAT has been demonstrated by retrograde tract tracing, electrophysiological recording and labelling of the sensory-associated neuropeptide calcitonin gene-related peptide in WAT. Local injections of the sensory nerve neurotoxin capsaicin into WAT selectively destroy this innervation. Just as surgical removal of WAT pads triggers compensatory increases in lipid accretion by non-excised WAT depots, capsaicin-induced sensory denervation triggers increases in lipid accretion of non-capsaicin-injected WAT depots, suggesting that these nerves convey information about body fat levels to the brain. Finally, parasympathetic nervous system innervation of WAT has been suggested, but the recent finding of no WAT immunoreactivity for the possible parasympathetic marker vesicular acetylcholine transporter (VAChT) argues against this claim. Collectively, these data suggest several roles for efferent and afferent neural innervation of WAT in body fat regulation.

Catecholaminergic innervation of white adipose tissue in Siberian hamsters

1995 ◽  
Vol 268 (3) ◽  
pp. R744-R751 ◽  
Author(s):  
T. G. Youngstrom ◽  
T. J. Bartness
Keyword(s):  
Adipose Tissue ◽  
White Adipose Tissue ◽  
Neural Control ◽  
Fat Pad ◽  
Anterograde Transport ◽  
Siberian Hamsters ◽  
Lipid Stores ◽  
Catecholaminergic Innervation ◽  
Fat Pads

When Siberian hamsters are transferred from long summerlike days (LDs) to short winterlike days (SDs) they decrease their body weight, primarily as body fat. These SD-induced decreases in lipid stores are not uniform. Internally located white adipose tissue (WAT) pads are depleted preferentially of lipid, whereas the more externally located subcutaneous WAT pads are relatively spared. These data suggest a possible differential sympathetic neural control over catecholamine-induced lipolysis and that lipolytic rates are greater for internal vs. external WAT pads. Moreover, if these differential rates of lipolysis are due to differential sympathetic nervous system (SNS) drives on the pads, then fat pad-specific catecholaminergic innervation may exist. Therefore, we tested whether inguinal WAT (IWAT; an external pad) and epididymal WAT (EWAT; an internal pad) were innervated differentially. In addition, we tested whether norepinephrine (NE) turnover (TO) reflected the presumed greater SNS drive on EWAT vs. IWAT after SD exposure. Injections of fluorescent tract tracers [Fluoro-Gold or indocarbocyanine perchlorate (DiI)] demonstrated projections from the SNS ganglia T13-L3 to both fat pads. Retrograde labeling revealed a relatively separate pattern of distribution of labeled neurons in the ganglia projecting to each pad. In vivo anterograde transport of DiI resulted in labeling in both IWAT and EWAT that included staining around individual adipocytes and occasionally retrogradely labeled cells. The proportionately greater decrease in EWAT compared with IWAT mass after 5 wk of SD exposure was reflected in greater EWAT NE TO than found in their LD counterparts for this pad.(ABSTRACT TRUNCATED AT 250 WORDS)

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
Keyword(s):  
Adipose Tissue ◽  
Body Fat ◽  
White Adipose Tissue ◽  
Sympathetic Innervation ◽  
Day Length ◽  
Sympathetic Denervation ◽  
Siberian Hamster ◽  
Siberian Hamsters ◽  
Length Changes ◽  
White Fat

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.

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