The endocannabinoid system: Body weight and metabolic regulation

Clinical Cornerstone • ABDOMINAL ADIPOSITY AND CARDIOMETABOLIC RISK • Vol. 8, Supplement 4

The Endocannabinoid System: Body Weight and Metabolic Regulation STEFAN ENGELI, MD, AND JENS JORDAN, M D Franz Volhard Clinical Research Center University Clinic Charit4 Campus Buch Humboldt University of Berlin Berlin, Germany

The endocannabinoid system elicits multiple physiologic functions that are not fully understood. Antagonism of cannabinoid type 1 (CB 1) receptors has been the only successful new pharmacologic treatment approach in Phase III studies in obesity in the last 8 years. Whereas antagonism of C B 1 receptors acutely reduces food intake, the long-term effects on weight reduction and metabolic regulation appear to be mediated by stimulation of energy expenditure and by peripheral effects related to liver, skeletal muscle, adipose tissue, and pancreas physiology. For example, in the liver, lipogenic enzymes and fatty acid synthesis are upregulated by endocannabinoids, and in adipose tissue, antagonism of CB 1 receptors increases secretion of adiponectin. Some studies suggest that endocannabinoid formation is increased in obesity, perhaps because endocannabinoid degradation is decreased. Although many questions remain unanswered at present, the emerging concept of endocannabinoids as metabolic regulators helps to explain the success of rimonabant (SR141716), an antagonist of CB 1 receptors, currently in Phase III studies. (Clinical Cornerstone. 2006;8[Suppl 4]:$24-$35). Copyright © 2006

Excerpta Medica, Inc.

The worldwide increase in the prevalence of obesity and

associated metabolic and cardiovascular diseases is a matter of increasing concern as more and more patients require treatment. 1,2 Successful use of nonpharmacolog-

ic therapy requires highly motivated patients and dedicat- ed teams of physicians, dietitians, and psychologists, 3 a strategy that is demanding for both patients and health

care providers. Because few patients attain long-term weight reduction and weight maintenance with nonphar- macologic therapy, 4 pharmacologic therapy will be used

increasingly more often and new pharmacologic treatment options are required. 5 7

In many therapeutic areas, the goal of drug development

has been to further refine the specificity of drugs and molecular targets. Nevertheless, recognition of the pleiotropic eflects of statins, angiotensin-receptor blockers,

or glitazones suggests that the approach to cardiovascular and metabolic risk modification in general may require a complex rather than a highly specific approach, s 10

The same observations may hold true for obesity treatment. Body weight reduction through a highly specific mechanism may not provide full metabolic and cardio-

vascular benefits. One possible approach is to define tar-

gets that lead to improved cardiovascular and metabol-

ic risk beyond the effect of weight reduction. The endocannabinoid system (ECS) may be such a target. Indeed, this system elicits multiple physiologic func-

tions that are not fully understood. ECS antagonism, however, has been the only successful new pharmacologic treatment approach in Phase III obesity studies in

the last 8 years. 11q3 This article provides an overview of the biology of the ECS and its involvement in obesity- associated disease.

The Endocannabinoid System: A Brief History Exogenous cannabinoids (CBs) contained in hemp

(Cannabis sativa) extracts and plant parts have been used for medical and recreational purposes for thou- sands of years. The principal chemical compound, delta9-tetrahydrocannabinol (A9-THC), was identified in 1964.14 The history of the ECS, however, is much more recent (Table). 11 34 The first CB receptor was cloned in

1990,16 and the first endocannabinoid--an endogenous CB receptor ligand--was discovered in 1992.18 The first

orally available selective receptor antagonist, rimonabant (SR141716), was described in 1994, 2o and the weight-

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TABLE. A BRIEF HISTORY OFTHE ENDO- CANNABINOID SYSTEM (ECS)fl 1-34

Year Discovery

1964 A°-THC identified 14

1 9 8 8 High-affnity cannabinoid (CB) binding sites in the brain identified 15

1990/1991 Rat CB 1 receptor clonedl6/human CB1 receptor cloned 17

1992 First endocannabinoid identifed: anandamide is

1 9 9 3 Peripheral CB 2 receptor cloned 1°

1994 First c g 1 antagonist developed: rimonabant 2°

1995 Second endocannabinoid identified: 2-AG 21'22

1996 Specific enzyme for anazldmnide degradation identified: F A A H 23

1 9 9 8 Rimonabant found to reduce body weight 24

1 9 9 9 Knockout (CB 14- ) mouse model engineered 25

2003-2006 Peripheral metabolic effects of the ECS discovered 2641

2 0 0 4 Endocannabinoids found to be neurotransmitters 32

2004 Specific enzyme for anandamide synthesis identified: NAPE-PLD 33

2005/2006 Results of RIO study published 11 13 Activation of the ECS in human obesity described 3°'34

cj cj k -THC = delta -tetrahydrocannabinol: C B 1 = cannabinoid type 1: CB~ = cannabinoid type 2: 2-AG = 2-arachidonoylglycerol: FA~H = fatty acid amide hydrolase: NAPE-PLD = N- acylphosphatidylethanolmnine phospholipase D: RIO = Rimonabant in Obesity.

reducing eflects of this compound in rats were reported for

the first time in 1998. 24 Although several important com-

ponents of the ECS, such as the putative endocannabinoid

membrane transporter, are yet to be discovered, the central

eflects of endocannabinoids have been recognized for cen-

turies. The role of endocannabinoids and their signal trans-

mission for the physiology of addiction, locomotion, pain,

and memory have been intensively studied. 25'32'35'36 More

recent discoveries acknowledge that CB receptors mediate

cardiovascular effects 37 and modulate inflammatory

responses. 3s The study of cannabinoid type 1 (CB1)- mediated eflects was stimulated by the discovery of the

specific inverse agonist/antagonist, rimonabant, 2° and the

development of specially bred mice with the CB 1 gene

deleted, known as CB 1 knockout (CB1 -/-) mice. 25

Endocannabinoid Synthesis and Degradat ion

Endocannabinoids are synthesized from phospholipid

derivatives of arachidonic acid. The 2 most important

endocannabinoids--anandamide (arachidonoylethanol-

amine) and 2-arachidonoylglycerol ( 2 -AG) - - a r e deriv-

ed f rom membrane phospholipids and triglycerides,

respectively. 39 Anandamide is synthesized by N-acyl-

phosphatidylethanolamine phospholipase D (NAPE-PLD)) 3

The process requires the preceding activity of N-acyl-

transferase to supply sufficient quantities of N-arachidonoyl-

phosphatidylethanolamine as a membrane-bound precursor

for NAPE-PLD. 39 Synthesis of 2-AG is a less specific

process. At least in the brain, 2-AG is an important

intermediate in several biochemical pathways and is

present at a concentration that is -200 times higher than

anandamide. 39 Thus, several enzymes not specifically

belonging to the ECS contribute to 2-AG synthesis.

K E Y P O I N T

The 2 most important endocannabinoids

manandamide and 2 -AGmare derived

from membrane phospholipids and

triglycerides, respectively.

One distinctive feature of endocannabinoids is "use-

dependent synthesis." In contrast to classical neurotrans-

mitters, endocannabinoids are not stored in vesicles.

Instead, they are synthesized on demand in response to

acute stimulation. The response is mediated through

increased intracellular calcium concentrations that initi-

ate endocannabinoid synthesis. 39

Endocannabinoid production and degradation occur

rapidly. After synthesis and release, endocannabinoids

are taken up again by a transporter that has not yet been

identified and then enzymatically degraded within the

cells. Anandamide is specifically degraded by fatty acid

amide hydrolase (FAAH). 39 FAAH gene expression has

been demonstrated recently in several human t issues-- in

the central nervous system (CNS) and in peripheral

organs. 34 This observation is indirect evidence for a

broad distribution of endocannabinoids throughout the

body. 2-AG is inactivated by a less specific e n z y m e - -

monoacylglycerol lipase, which is present in

adipocytes-- to facilitate release of nonesterified fatty

acids. 4° Monoacyglycerol lipase was first characterized

as part of the ECS in the mouse brain in 2002. 40

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Endocannabinoid Receptors

Endocannabinoids bind to G-protein-coupled receptors, namely the CB 1 and cannabinoid type 2 (CB2) receptors. CB~ receptors represent the single most abundant receptor

type in the mammalian CNS and are found in several brain regions--the olfactory bulb, cerebellum, cortex, hypothal- amus, nucleus accumbens, basal ganglia, and spinal cord. 41

Surprisingly, recent studies revealed that CB 1 receptors are also present in peripheral tissues, such as the gastrointes- tinal tract, liver, adipose tissue, skeletal muscle, testes, uterus, placenta, and bone. 26 28,34,42-44 C B 1 receptors are

expressed on endothelial cells as well, 45 and this may con-

tribute to positive CB 1 signals in whole-organ prepara-

tions. 34 In human and rodent adipose tissue, CB~ expression is stronger in adipocytes than in other cell types, including preadipocytes, suggesting that CB 1 receptors contribute to the phenotype of mature adipocytes. 28'29'34

CB 2 receptors are predominantly expressed on peripheral immune cells, 41 but they recently have also been described in mouse liver .6 and human adipocytes. 47 The role of CB 2

for adipocyte biology and metabolic regulation remains completely unknown at present.

A typical response to CB-receptor activation is inhibition of adenylate cyclase activity, resulting in reduced intracellular cyclic adenosine monophosphate (cAMP)

levels. 41 However, other second messenger systems, such as protein kinases and transcription factors, are involved as well. On the molecular level, retrograde signaling is an important part of endocannabinoid action. 32'39 Retro-

grade signaling refers to the fact that CB1 receptors are located on presynaptic neurons, whereas the activating

endocannabinoids are produced by postsynaptic neurons (Figure 1). 4s Through retrograde signaling, postsynaptic

terminals of specific neurons modulate presynaptic neu-

rotransmitter release via endocannabinoids and CB~ receptors, which inhibits calcium channels and opens potassium channels. Inhibition of neurotransmitter

release by presynaptic CB~ receptors has been shown for acetylcholine, norepinephrine, serotonin, glutamate, and cholecystokinin. In contrast, dopamine release appears to

be enhanced by CB~ receptors in certain parts of the brain. 32'39 The significance of each endocannabinoid sig-

naling pathway, however, needs to be specified in each

organ or cell of interest, and these data are currently missing for most peripheral organs. Whether retrograde signaling also occurs in peripheral tissues (eg, modula-

tion of norepinephrine or acetylcholine release from

autonomic neurons by endocannabinoids produced by

target cells) remains a matter of debate.

Endocannabinoids, Food Intake,

and Body W e i g h t Exogenous CBs and endocannabinoids increase food

intake and promote weight gain in experimental animals through activation of central CB 1 receptors. 49 51 In-

terestingly, food intake can be induced even in animals that have already been fed and by administration of endo-

cannabinoids in brain regions not directly involved in food intake, for example, the nucleus accumbens. 52

Furthermore, endocannabinoid levels in the hypothala-

mus increase with fasting and are rapidly suppressed by feeding. 52 The influence of endocannabinoids on feeding

behavior is attributable, in part, to interactions with the

stomach-derived hormone ghrelin. The orexigenic effects of centrally administered ghrelin were abolished by rimonabant, suggesting that ghrelin acts, at least in part,

by increasing endocannabinoid production in the hypo- thalamus. 53 However, the response of circulating ghrelin

to fasting was also diminished by rimonabant, suggesting that CB 1 receptors are also involved in ghrelin secretion. 54

Overall, these findings clearly demonstrate that endocannabinoids have a role in the control of all aspects of food intake, 55 a phenomenon that has been exploited in the medical treatment of cachexia using A9-THC. 56

Consistent with the effects of endocannabinoids on

feeding behavior are the results of studies with CB(/- mice and rimonabant with respect to body weight changes. CB{/- mice are lean and resistant to diet- induced obesity. 57 Body weight and body fat mass of

CB(/- mice are approximately 24% and 60% lower than wildtype (CBI+/+) mice, respectively. The lean phenotype

is associated with changes in the balance between orexigenic and anorexigenic systems within the CNS. In CB{/- mice, hypothalamic expression of the anorexigenic

gene--corticotropin-releasing hormone--is increased. Expression of the orexigenic gene--cocaine- and amphetamine-related transcript (CART)--is decreased. 29

These findings may explain, in part, the body weight reduction in CB{/- mice. Recent studies also demonstrated that CB~ activation in CB~ +/+ mice increased CART

expression in hypothalamic nuclei and the nucleus accumbens, again suggesting that CART is a downstream medi- ator of orexigenic endocannabinoid actions. 5s Similar to

genetic inactivation of CB 1 receptors, pharmacologic CB 1

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