Dysregulation of Leptin in Response to Fasting in Insulin-Resistant
Psammomys Obesus (Israeli sand rats)
Ken Walder, Scott Lee, Paul Zimmet, and Greg R. Collier
Leptin is thought to play a significant role in energy balance as an afferent signal to the hypothalamus that reflects body fat
content. In addition, leptin may also act as an acute sensor of energy balance independent of body fat mass, since ob gene
expression and plasma leptin concentrations are decreased in lean animals and humans in response to short-term caloric
deprivation. However, in obese animals and humans, the acute response of leptin to fasting is less clear. We investigated the
effects of a 24-hour fast on circulating plasma leptin concentrations in lean and obese Psammomys obesus (Israeli sand rats). In
the lean, insulin-sensitive group (n = 25) a 24-hour fast caused a 44% decrease in plasma leptin, whereas in the obese,
insulin-resistant group (n = 24) plasma leptin increased by 18% after fasting (P < .003). There was no difference between the
two groups regarding the effect of a 24-hour fast on body weight, blood glucose, or plasma insulin. Within the insulin-resistant
group, there was no difference in the response of leptin to fasting between hyperglycemic and normoglycemic animals. We
conclude that there is a dysregulation of leptin in response to acute caloric deprivation in obese, insulin-resistant but not in
lean, insulin-sensitive P obesus.
Copyright© 1998by W.B. Saunders Company
L
EPTIN, the product of the ob gene, is secreted exclusively
from adipocytes and is thought to play an important role
in the regulation of energy metabolism and body weight. 1 The
hyperphagia, obesity, and insulin resistance that characterize the
ob/ob mouse phenotype were all shown to be rapidly reversed
by leptin administration, which also caused significant weight
loss in wild-type mice. 2-4
Numerous studies in both humans 54 and animal models of
obesity other than ob/ob mice 2-4,9,1° have demonstrated that ob
gene expression and plasma leptin concentrations reflect body
fat mass, and suggest that leptin may act as an afferent signal to
the brain influencing energy balance.
The proposal that leptin plays an important role in the control
of energy balance and utilization has led to interest in the
short-term regulation of ob gene expression and the circulating
plasma leptin concentration. In wild-type mice, fasting for 48 to
72 hours decreased plasma leptin by 60% to 70%, 11,12while ob
gene expression decreased by 85% after a 16-hour fast 13 and
90% after a 48-hour fast. TM In lean control rats, fasts of 16 to 72
hours' duration decreased plasma leptin by 50% to 80%. 13J5-17
Similarly, in lean humans, fasting for 24 to 60 hours caused a
60% to 70% reduction in plasma leptin. 18-2° It appears that
fasting significantly reduces ob gene expression and plasma
leptin in lean, healthy animals and humans.
In obesity, the response of leptin to fasting is less clear.
Fasting did not significantly reduce ob gene expression in ob/ob
mice after 16 hours, in diet-induced obese mice after 48 hours,
or in fa/fa rats after 72 hours. 13,14,16 However, several small
studies in obese humans have shown that fasting for 24 to 60
hours reduced circulating plasma leptin by 42% to 88 %.t8-2° To
further clarify this, we investigated the response of leptin to a
24-hour fast in a polygenic, heterogeneous model of obesity and
non-insulin-dependent diabetes mellitus (NIDDM), Psammo-
mys obesus (the Israeli sand rat).
P obesus is a unique animal model of obesity and NIDDM. P
obesus remains lean and normoglycemic in the wild on its
natural low-energy diet. 2I However, when taken into the
laboratory and fed ad libitum chow, a relatively energy-dense
food, the animals exhibit a range of pathophysiological re-
sponses, with approximately half becoming obese and about
one third developing NIDDM. 22,23 P obesus exhibits a range of
body weight and blood glucose and insulin concentrations that
form a continuous curve, closely resembling the pattern found
in human population. 22,24 It is the heterogeneity of the pheno-
typic response of P obesus that makes it a useful model to study
the etiology and pathophysiology of obesity and NIDDM.
The aim of this study was to investigate the response of leptin
to a 24-hour fast in P obesus with a wide range of body weight
and circulating glucose and insulin concentrations.
MATERIALS AND METHODS
Breeding of the Colony
A P. obesus colony is maintained at Deakin University, with the
breeding pairs fed ad iibitum a diet of alfalfa and standard laboratory
chow. Experimental animals were weaned at 4 weeks of age and
sustained on a diet of standard laboratory chow from which 12% of the
energy was derived from fat, 63% from carbohydrate, and 25% from
protein (Barastoc, Pakenham, Australia). The animals were housed in a
humidity- and temperature-controlled room (22° + 1°C) with a 12-hour
light-dark cycle. The animals used in the study were 12 to 14 weeks of
age when fasted.
Experimental Protocol
The animals (N = 49) were weighed and blood was coIlected from
the tail vein in the fed state. They were then fasted for 24 hours before
being weighed again, and blood was collected again in the fasted state.
The animals were evaluated for a further 28 days with ad libitum access
to food and water before being weighed and bled again. All blood was
collected into heparinized tubes. The experiments were performed
following the Australian National Health and Medical Research Council
principles of laboratory animal care, and were approved by the Deakin
University Animal Ethics Committee.
From the School of Nutrition and Public Health, Deakin University,
Geelong; and the International Diabetes Institute, Caulfield, Australia.
Submitted May 8, 1997; accepted June 25, 1997.
Supported in part by the National Health and Medical Research
Council of Australia and Deakin University Internal Research Grants.
Address reprint requests to Greg R. Collier, PhD, School of Nutrition
and Public Health, Deakin University, Geelong, Victoria, Australia
3216.
Copyright © 1998 by W..B.Saunders Company
0026-0495/98/4701-0024503.00/0
Metabolism, Vo147, No 1 (January), 1998: pp 125-128 125