TRENDSin Endocrinology & Metabolism Vol.13 No.1 January/February 2002
http://tem.trends.com 1043-2760/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1043-2760(01)00522-7
18 Review
Insulin resistance is defined as a failure of target
tissues (adipose, liver, skeletal and cardiac muscle) to
respond normally to insulin [1]. At the molecular
level, this resistance can occur anywhere in the
insulin signaling pathway, from receptor binding to
downstream signaling events. Obesity-associated
insulin resistance is manifested by increased hepatic
glucose output and reduced glucose disposal in
peripheral tissues at a given level of insulin [2].
Quantitatively, skeletal muscle is the most important
site of insulin-mediated glucose disposal [3]. Adipose
tissue clearly plays a significant role in the
pathogenesis of insulin resistance, as shown by the
high correlation between obesity and insulin
resistance [2]. Obesity-induced insulin resistance is
affected both by the total amount of adipose tissue
and its distribution [4]. Both visceral and deep
subcutaneous adipose tissues are associated with
insulin resistance [5]. Excessive free fatty acids
(FFAs) released by lipolysis from adipose tissue have
been implicated in non-insulin dependent diabetes
mellitus. FFAs compete with glucose for oxygen and
inhibit whole body glucose disposal via the ‘Randle
cycle’ [6]. FFAs have a deleterious effect on insulin
uptake by the liver and contribute to the increased
hepatic glucose release [7]. The concept that signals
emanating from adipose tissue regulate organismal
glucose homeostasis has been reinforced by the
observation that adipose-specific changes in gene
expression alter insulin sensitivity in muscle and
liver in the mouse [8].
Adipose tissue as an endocrine organ
Adipose tissue is the body’s largest reserve of fuel,
storing energy in the form of triacylglycerides. This
energy can be rapidly mobilized during starvation and
other times of need. The switch from energy storage to
mobilization within adipocytes is regulated by
hormonal signals from other tissues and organs,
including the pancreas (insulin), the sympathetic
nervous system (catecholamines) and the adrenal
glands (glucocorticoids). Until recently, adipocytes were
viewed as playing a passive role in fuel homeostasis,
with obesity being a consequence of chronic positive
energy balance. However, it is now recognized that the
endocrine function of adipose tissue is a crucial
determinant of energy balance. The discovery of leptin
as an adipocyte-derived peptide hormone, the absence
of which causes massive obesity in mice [9] and humans
[10], conclusively established the endocrine function of
adipose tissue. Characterization of the leptin receptor
and its mutation in obese mice [11] and people [12]
reinforced the notion of adipocytes as a key component
of a classical endocrine system with the hypothalamus
as a major target tissue [13]. The actions of leptin on the
brain include not only regulation of satiety [14–16] but
also efferent pathways controlling metabolism [17] and
other endocrine systems involved in the starvation
response [18].
The discovery of the leptin endocrine system
triggered a conceptual shift leading to increased
interest in other adipocyte products as signaling
molecules. These include FFAs, the elevated levels of
which in obesity are probably causally related to
reduced insulin action in peripheral tissues [19]. In
addition, increasing numbers of proteins are being
found to be secreted by adipose tissue, including
Acrp30/adiponectin/AdipoQ (herein referred to as
Acrp30) [20–22], tumor necrosis factor α (TNF-α) [23],
adipsin [24], plasminogen activator-inhibitor [25],
acylation-stimulating protein [26], interleukin 6
(IL-6) [27], IL-8 [28], agouti protein [29], transforming
growth factor β [30], angiotensinogen [31] and
adipophilin [32]. Many of these cytokines and
hormones are potential regulators of glucose
homeostasis. This review of potential mediators of
obesity-associated insulin resistance focuses on the
polypeptides that have received the most recent
attention, namely: leptin, TNF-α, Acrp30 and IL-6.
Potential mediators of obesity-associated insulin
resistance
Leptin
Leptin regulates food intake, body weight, energy
expenditure and neuroendocrine function [33,34].
Obesity is a major risk factor for insulin resistance and type 2 diabetes mellitus.
Adipocytes secrete numerous substances that might contribute to peripheral
insulin sensitivity.These include leptin,tumor necrosis factor α,
Acrp30/ adiponectin/ adipoQ and interleukin 6, the potential roles of which are
briefly reviewed here. Thiazolidinedione (TZD) antidiabetic drugs regulate gene
transcription by binding to peroxisome proliferator activated receptor γ,a
nuclear hormone receptor found at its highest levels in adipocytes. A search for
genes that are downregulated by TZDs in mouse adipocytes led to the
discovery of an adipose-specific secreted protein called resistin. Resistin
circulates in the mouse, with increased levels in obesity, and has effects on
glucose homeostasis that oppose those of insulin. Thus, resistin is a potential
link between TZDs, obesity and insulin resistance in the mouse. Future studies
must address the mechanism of action and biological role of resistin and
related family members in mice and humans.
Claire M. Steppan
Mitchell A. Lazar*
Division of
Endocrinology, Diabetes,
and Metabolism, Depts of
Medicine and Genetics
and The Penn Diabetes
Center, University of
Pennsylvania Medical
Center, Philadelphia,
PA 19104-6149, USA.
* e-mail: lazar@
mail.med.upenn.edu
Resistin and obesity-associated
insulin resistance
Claire M. Steppan and Mitchell A. Lazar