scholarly journals The Importance of Peripheral Nerves in Adipose Tissue for the Regulation of Energy Balance

Biology ◽  
2019 ◽  
Vol 8 (1) ◽  
pp. 10 ◽  
Author(s):  
Magdalena Blaszkiewicz ◽  
Jake W. Willows ◽  
Cory P. Johnson ◽  
Kristy L. Townsend
Keyword(s):  
Adipose Tissue ◽  
Energy Balance ◽  
Peripheral Nerves ◽  
Uncoupling Protein ◽  
Sympathetic Nerves ◽  
Cell Types ◽  
Nerve Fibers ◽  
Sensory Nerves ◽  
Brown Adipose ◽  
The Brain

Brown and white adipose tissues are essential for maintenance of proper energy balance and metabolic health. In order to function efficiently, these tissues require both endocrine and neural communication with the brain. Brown adipose tissue (BAT), as well as the inducible brown adipocytes that appear in white adipose tissue (WAT) after simulation, are thermogenic and energy expending. This uncoupling protein 1 (UCP1)-mediated process requires input from sympathetic nerves releasing norepinephrine. In addition to sympathetic noradrenergic signaling, adipose tissue contains sensory nerves that may be important for relaying fuel status to the brain. Chemical and surgical denervation studies of both WAT and BAT have clearly demonstrated the role of peripheral nerves in browning, thermogenesis, lipolysis, and adipogenesis. However, much is still unknown about which subtypes of nerves are present in BAT versus WAT, what nerve products are released from adipose nerves and how they act to mediate metabolic homeostasis, as well as which cell types in adipose are receiving synaptic input. Recent advances in whole-depot imaging and quantification of adipose nerve fibers, as well as other new research findings, have reinvigorated this field of research. This review summarizes the history of research into adipose innervation and brain–adipose communication, and also covers landmark and recent research on this topic to outline what we currently know and do not know about adipose tissue nerve supply and communication with the brain.

Brown Adipose Tissue: Function and Physiological Significance

2004 ◽  
Vol 84 (1) ◽  
pp. 277-359 ◽  
Author(s):  
BARBARA CANNON ◽  
JAN NEDERGAARD
Keyword(s):  
Adipose Tissue ◽  
Brown Adipose Tissue ◽  
Heat Production ◽  
Uncoupling Protein ◽  
Sympathetic Nerves ◽  
Physiological Significance ◽  
Metabolic Efficiency ◽  
Transfer Energy ◽  
Brown Adipose ◽  
Evolutionary Success

Cannon, Barbara, and Jan Nedergaard. Brown Adipose Tissue: Function and Physiological Significance. Physiol Rev 84: 277–359, 2004; 10.1152/physrev.00015.2003.—The function of brown adipose tissue is to transfer energy from food into heat; physiologically, both the heat produced and the resulting decrease in metabolic efficiency can be of significance. Both the acute activity of the tissue, i.e., the heat production, and the recruitment process in the tissue (that results in a higher thermogenic capacity) are under the control of norepinephrine released from sympathetic nerves. In thermoregulatory thermogenesis, brown adipose tissue is essential for classical nonshivering thermogen-esis (this phenomenon does not exist in the absence of functional brown adipose tissue), as well as for the cold acclimation-recruited norepinephrine-induced thermogenesis. Heat production from brown adipose tissue is activated whenever the organism is in need of extra heat, e.g., postnatally, during entry into a febrile state, and during arousal from hibernation, and the rate of thermogenesis is centrally controlled via a pathway initiated in the hypothalamus. Feeding as such also results in activation of brown adipose tissue; a series of diets, apparently all characterized by being low in protein, result in a leptin-dependent recruitment of the tissue; this metaboloregulatory thermogenesis is also under hypothalamic control. When the tissue is active, high amounts of lipids and glucose are combusted in the tissue. The development of brown adipose tissue with its characteristic protein, uncoupling protein-1 (UCP1), was probably determinative for the evolutionary success of mammals, as its thermogenesis enhances neonatal survival and allows for active life even in cold surroundings.

Selenium and iodine deficiencies: effects on brain and brown adipose tissue selenoenzyme activity and expression

1997 ◽  
Vol 155 (2) ◽  
pp. 255-263 ◽  
Author(s):  
JH Mitchell ◽  
F Nicol ◽  
GJ Beckett ◽  
Keyword(s):  
Adipose Tissue ◽  
Thyroid Hormone ◽  
Glutathione Peroxidase ◽  
Brown Adipose Tissue ◽  
Iodine Deficiency ◽  
Uncoupling Protein ◽  
Compensatory Mechanisms ◽  
Iodothyronine Deiodinase ◽  
Brown Adipose ◽  
The Brain

Adequate dietary iodine supplies and thyroid hormones are needed for the development of the central nervous system (CNS) and brown adipose tissue (BAT) function. Decreases in plasma thyroxine (T4) concentrations may increase the requirement for the selenoenzymes types I and II iodothyronine deiodinase (ID-I and ID-II) in the brain and ID-II in BAT to protect against any fall in intracellular 3,3',5 tri-iodothyronine (T3) concentrations in these organs. We have therefore investigated selenoenzyme activity and expression and some developmental markers in brain and BAT of second generation selenium- and iodine-deficient rats. Despite substantial alterations in plasma thyroid hormone concentrations and thyroidal and hepatic selenoprotein expression in selenium and iodine deficiencies, ID-I, cytosolic glutathione peroxidase (cGSHPx) and phospholipid hydroperoxide glutathione peroxidase (phGSHPx) activities and expression remained relatively constant in most brain regions studied. Additionally, brain and pituitary ID-II activities were increased in iodine deficiency regardless of selenium status. This can help maintain tissue T3 concentrations in hypothyroidism. Consistent with this, no significant effects of iodine or selenium deficiency on the development of the brain were observed, as assessed by the activities of marker enzymes. In contrast, BAT from selenium- and iodine deficient rats had impaired thyroid hormone metabolism and less uncoupling protein than in tissue from selenium- and iodine-supplemented animals. Thus, the effects of selenium and iodine deficiency on the brain are limited due to the activation of the compensatory mechanisms but these mechanisms are less effective in BAT.

scholarly journals Adipose tissue development during early life: novel insights into energy balance from small and large mammals

2012 ◽  
Vol 71 (3) ◽  
pp. 363-370 ◽  
Author(s):  
Michael E. Symonds ◽  
Mark Pope ◽  
Helen Budge
Keyword(s):  
Adipose Tissue ◽  
Energy Balance ◽  
Cold Exposure ◽  
Early Life ◽  
Uncoupling Protein ◽  
Human Subjects ◽  
Tissue Type ◽  
Brown Adipose ◽  
Organ Specific ◽  
Adipose Tissue Development

Since the rediscovery of brown adipose tissue (BAT) in adult human subjects in 2007, there has been a dramatic resurgence in research interest in its role in heat production and energy balance. This has coincided with a reassessment of the origins of BAT and the suggestion that brown preadipocytes could share a common lineage with skeletal myoblasts. In precocial newborns, such as sheep, the onset of non-shivering thermogenesis through activation of the BAT-specific uncoupling protein 1 (UCP1) is essential for effective adaptation to the cold exposure of the extra-uterine environment. This is mediated by a combination of endocrine adaptations which accompany normal parturition at birth and further endocrine stimulation from the mother's milk. Three distinct adipose depots have been identified in all species studied to date. These contain either primarily white, primarily brown or a mix of brown and white adipocytes. The latter tissue type is present, at least, in the fetus and, thereafter, appears to take on the characteristics of white adipose tissue during postnatal development. It is becoming apparent that a range of organ-specific mechanisms can promote UCP1 expression. They include the liver, heart and skeletal muscle, and involve unique endocrine systems that are stimulated by cold exposure and/or exercise. These multiple pathways that promote BAT function vary with age and between species that may determine the potential to be manipulated in early life. Such interventions could modify, or reverse, the normal ontogenic pathway by which BAT disappears after birth, thereby facilitating BAT thermogenesis through the life cycle.

scholarly journals Leptin Modulates the Response of Brown Adipose Tissue to Negative Energy Balance: Implication of the GH/IGF-I Axis

2021 ◽  
Vol 22 (6) ◽  
pp. 2827
Author(s):  
Vicente Barrios ◽  
Laura M. Frago ◽  
Sandra Canelles ◽  
Santiago Guerra-Cantera ◽  
Eduardo Arilla-Ferreiro ◽  
...  
Keyword(s):  
Adipose Tissue ◽  
Energy Balance ◽  
Brown Adipose Tissue ◽  
Uncoupling Protein ◽  
Negative Energy ◽  
Negative Energy Balance ◽  
Cytokine Signaling ◽  
Mrna Levels ◽  
Brown Adipose ◽  
Igf I

The growth hormone (GH)/insulin-like growth factor I (IGF-I) axis is involved in metabolic control. Malnutrition reduces IGF-I and modifies the thermogenic capacity of brown adipose tissue (BAT). Leptin has effects on the GH/IGF-I axis and the function of BAT, but its interaction with IGF-I and the mechanisms involved in the regulation of thermogenesis remains unknown. We studied the GH/IGF-I axis and activation of IGF-I-related signaling and metabolism related to BAT thermogenesis in chronic central leptin infused (L), pair-fed (PF), and control rats. Hypothalamic somatostatin mRNA levels were increased in PF and decreased in L, while pituitary GH mRNA was reduced in PF. Serum GH and IGF-I concentrations were decreased only in PF. In BAT, the association between suppressor of cytokine signaling 3 and the IGF-I receptor was reduced, and phosphorylation of the IGF-I receptor increased in the L group. Phosphorylation of Akt and cyclic AMP response element binding protein and glucose transporter 4 mRNA levels were increased in L and mRNA levels of uncoupling protein-1 (UCP-1) and enzymes involved in lipid anabolism reduced in PF. These results suggest that modifications in UCP-1 in BAT and changes in the GH/IGF-I axis induced by negative energy balance are dependent upon leptin levels.

Sex-related differences in energy balance in response to caloric restriction

2005 ◽  
Vol 289 (1) ◽  
pp. E15-E22 ◽  
Author(s):  
A. Valle ◽  
A. Català-Niell ◽  
B. Colom ◽  
F. J. García-Palmer ◽  
J. Oliver ◽  
...  
Keyword(s):  
Energy Efficiency ◽  
Adipose Tissue ◽  
Energy Balance ◽  
Caloric Restriction ◽  
Uncoupling Protein ◽  
Caloric Intake ◽  
Carbon Dioxide Production ◽  
Brown Adipose ◽  
Ad Libitum ◽  
Ad Libitum Intake

Sex-related differences in energy balance were studied in young Wistar rats fed standard chow pellets either ad libitum or in restricted amounts (60% of ad libitum intake) for 100 days. Caloric intake, indirect calorimetry, organ and adipose tissue weights, energy efficiency, liver mitochondrial respiration rate, and brown adipose tissue (BAT) uncoupling protein-1 (UCP1) content were measured. Ad libitum-fed females showed greater oxygen consumption (V̇o2) and carbon dioxide production (V̇co2) and lower energy efficiency than males. Caloric restriction induced a chronic drop of V̇o2 and V̇co2 in females but not in males over the period studied. Restricted females showed a better conservation of metabolic active organ mass and a greater decrease in adipose depots than restricted males. Moreover, changes of BAT size and UCP1 content suggest that BAT may be the main cause responsible for sex differences in the response of energy balance to caloric restriction. In conclusion, our results indicate that females under caloric restriction conditions deactivate facultative thermogenesis to a greater degree than males. This ability may have obvious advantages for female survival and therefore the survival of the species when food is limiting.

Identification of brown fat and mechanisms for energy balance in the marsupial, Sminthopsis crassicaudata

1997 ◽  
Vol 273 (1) ◽  
pp. R161-R167 ◽  
Author(s):  
P. J. Hope ◽  
D. Pyle ◽  
C. B. Daniels ◽  
I. Chapman ◽  
M. Horowitz ◽  
...  
Keyword(s):  
Adipose Tissue ◽  
Energy Balance ◽  
Uncoupling Protein ◽  
Short Term ◽  
Mitochondrial Uncoupling ◽  
Carbohydrate Utilization ◽  
Mitochondrial Uncoupling Protein ◽  
Sminthopsis Crassicaudata ◽  
Brown Adipose ◽  
Ad Libitum

The presence of brown adipose tissue (BAT) in marsupials is controversial because attempts to identify mitochondrial uncoupling protein (UCP) have been unsuccessful. Sminthopsis crassicaudata is a small nocturnal marsupial with an interscapular pad of adipose tissue. Electron microscopy revealed this tissue to have characteristics typical of BAT. GDP binding and UCP detection by immunoblot confirmed BAT. Expression of UCP was increased by cold exposure. When animals were placed from 28 to 15 degrees C, body temperature (Tb) decreased by 1.7 degrees C within 30 min and a further 1.0 degree C by 90 min (P < 0.001) before stabilizing at these lower levels. When animals were returned to 28 degrees C, Tb increased within 30 min (P < 0.001) and returned to basal by 120 min. When animals were maintained at 15 degrees C with ad libitum food for 12 days, Tb (P < 0.05), tail width (P < 0.04), and O2 consumption (P < 0.01) all decreased. The respiratory quotient increased (P < 0.001), indicating a change from fat to carbohydrate utilization. Food intake was unchanged, and body weight increased on day 1 (P < 0.01) before returning to baseline on day 3, remaining stable thereafter. These data suggest that although BAT is present in the marsupial S. crassicaudata, it may not be necessary for thermogenesis, at least in the short term. S. crassicaudata utilizes a plasticity in Tb and a change in substrate utilization to maintain energy balance and body composition without the need for an increase in metabolic rate or food consumption and without the need for torpor.

scholarly journals The adipose organ: morphological perspectives of adipose tissues

2001 ◽  
Vol 60 (3) ◽  
pp. 319-328 ◽  
Author(s):  
Saverio Cinti
Keyword(s):  
Adipose Tissue ◽  
Uncoupling Protein ◽  
Gross Anatomy ◽  
Cell Types ◽  
Vascular Supply ◽  
Adipose Tissues ◽  
White Adipocyte ◽  
Metabolic Functions ◽  
Brown Adipose ◽  
Adipose Organ

Anatomically, an organ is defined as a series of tissues which jointly perform one or more interconnected functions. The adipose organ qualifies for this definition as it is made up of two tissue types, the white and brown adipose tissues, which collaborate in partitioning the energy contained in lipids between thermogenesis and the other metabolic functions. In rats and mice the adipose organ consists of several subcutaneous and visceral depots. Some areas of these depots are brown and correspond to brown adipose tissue, while many are white and correspond to white adipose tissue. The number of brown adipocytes found in white areas varies with age, strain of animal and environmental conditions. Brown and white adipocyte precursors are morphologically dissimilar. Together with a rich vascular supply, brown areas receive abundant noradrenergic parenchymal innervation. The gross anatomy and histology of the organ vary considerably in different physiological (cold acclimation, warm acclimation, fasting) and pathological conditions such as obesity; many important genes, such as leptin and uncoupling protein-1, are also expressed very differently in the two cell types. These basic mechanisms should be taken into account when addressing the physiopathology of obesity and its treatment.

scholarly journals Turning WAT into BAT: a review on regulators controlling the browning of white adipocytes

2013 ◽  
Vol 33 (5) ◽  
Author(s):  
Kinyui Alice Lo ◽  
Lei Sun
Keyword(s):  
Adipose Tissue ◽  
Energy Balance ◽  
Uncoupling Protein ◽  
Transcriptional Regulators ◽  
Peroxisome Proliferator ◽  
Uncoupling Protein 1 ◽  
Peroxisome Proliferator Activated Receptor ◽  
White Adipocytes ◽  
Brown Adipose ◽  
Pr Domain

Adipose tissue has a central role in the regulation of energy balance and homoeostasis. There are two main types of adipose tissue: WAT (white adipose tissue) and BAT (brown adipose tissue). WAT from certain depots, in response to appropriate stimuli, can undergo a process known as browning where it takes on characteristics of BAT, notably the induction of UCP1 (uncoupling protein 1) expression and the presence of multilocular lipid droplets and multiple mitochondria. How browning is regulated is an intense topic of investigation as it has the potential to tilt the energy balance from storage to expenditure, a strategy that holds promise to combat the growing epidemic of obesity and metabolic syndrome. This review focuses on the transcriptional regulators as well as various proteins and secreted mediators that have been shown to play a role in browning. Emphasis is on describing how many of these factors exert their effects by regulating the three main transcriptional regulators of classical BAT development, namely PRDM16 (PR domain containing 16), PPARγ (peroxisome proliferator-activated receptor γ) and PGC-1α (peroxisome proliferator-activated receptor γ coactivator 1α), which have been shown to be the key nodes in the regulation of inducible brown fat.

Thermogenesis and the energetics of pregnancy and lactation

1989 ◽  
Vol 67 (4) ◽  
pp. 370-375 ◽  
Author(s):  
P. Trayhurn
Keyword(s):  
Adipose Tissue ◽  
Energy Balance ◽  
Brown Adipose Tissue ◽  
Sympathetic Activity ◽  
Uncoupling Protein ◽  
Energy Utilization ◽  
Maximum Efficiency ◽  
Main Site ◽  
Brown Adipose ◽  
Rats And Mice

Energy balance studies suggest that the overall efficiency of energy utilization does not increase during pregnancy in rodents, other than as a consequence of "hyperphagia." Diet-induced thermogenesis is not stimulated in response to the increased energy intake of the pregnant animal, the extra intake being retained at the maximum efficiency. Biochemical studies on brown adipose tissue, the main site of adaptive thermogenesis in rodents, are consistent with the energy balance data, at least in rats and mice. However, in hamsters (golden and Djungarian) some atrophy of the tissue is evident during pregnancy. In contrast to pregnancy, the thermogenic activity (mitochondrial GDP binding) and capacity (uncoupling protein content) of brown adipose tissue are substantially reduced during lactation in rats and mice. These changes result from a fall in sympathetic activity in the tissue in lactation. Sympathetic activity and thermogenic capacity are, however, fully restored following weaning of the pups. The functional atrophy of brown adipose tissue during lactation is linked to a substantial saving in maternal energy expenditure, reducing the energy requirements for milk production. The lactating–post-lactating animal provides an excellent example of a physiologically programmed reversible atrophy of brown adipose tissue.Key words: brown adipose tissue, thermogenesis, pregnancy, lactation, energetics.

Rapid but transient atrophy of brown adipose tissue in capsaicin-desensitized rats

1992 ◽  
Vol 262 (4) ◽  
pp. R562-R567 ◽  
Author(s):  
J. Cui ◽  
J. Himms-Hagen
Keyword(s):  
Adipose Tissue ◽  
Brown Adipose Tissue ◽  
Body Weight Gain ◽  
Uncoupling Protein ◽  
Sensory Nerves ◽  
Epididymal Adipose Tissue ◽  
Inhibitory Influence ◽  
Trophic Effect ◽  
Brown Adipose ◽  
Sensory Neuropeptides

Our previous studies showed atrophy of brown adipose tissue (BAT) in capsaicin-desensitized rats during the period 11-28 days after injections [Cui et al., Am. J. Physiol. 259 (Regulatory Integrative Comp. Physiol. 28): R324-R332, 1990]. The objective of the present studies was to assess the rapidity with which the atrophy occurred and the extent to which recovery had occurred by 8 wk. Rats, either vehicle-injected controls or capsaicin injected, were studied 1, 3, 14, 28, and 52 days after the last injection. BAT was markedly atrophied at 1 day, having less total protein, fewer mitochondria (less total cytochrome oxidase and total uncoupling protein), and fewer cells (less DNA). Atrophy persisted for up to 14 days but had largely disappeared by 28-52 days. A transient reduction in body weight gain and white epididymal adipose tissue weight had also reversed by 28-52 days. We suggest that the rapid atrophy of BAT after capsaicin desensitization is secondary to the loss of sensory neuropeptides in its sensory nerves, neuropeptides that either exert a trophic effect on synthesis of mitochondria or an inhibitory influence on processes that promote degradation of mitochondria. The retardation of the normal age-associated increase in DNA content of BAT in the capsaicin-desensitized rat suggests that sensory neuropeptides might also modulate cell proliferation.

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