Are Peroxisome Proliferator-Activated Receptors Involved in Skeletal
Muscle Wasting during Experimental Cancer Cachexia?
Role of B
2
-Adrenergic Agonists
Gemma Fuster, Sı ´lvia Busquets, Elisabet Ametller, Mireia Olivan, Vanessa Almendro,
Cibely Cristine Fontes de Oliveira, Maite Figueras, Francisco J. Lo ´pez-Soriano,
and Josep M. Argile ´s
Cancer Research Group, Departament de Bioquı ´mica i Biologia Molecular, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain
Abstract
Implantation of the Yoshida AH-130 ascites hepatoma to rats
resulted in a decrease in muscle weight 7 days after the
inoculation of the tumor. These changes were associated with
increases in the mRNA content for both peroxisome prolifer-
ator-activatedreceptor(PPAR) ; andPPARD inskeletalmuscle.
The increase in gene expression for these transcription factors
was related to increases in the expression of several genes
involved in fatty acid transport, activation, and oxidation.
TumorburdenalsoresultedinincreasesinPPAR; coactivator-
1A gene expression and pyruvate dehydrogenase kinase 4. All
these changes in lipid metabolism genes suggest that a
metabolicshiftoccursinskeletalmuscleoftumor-bearingrats
toward a more oxidative phenotype. Formoterol treatment to
tumor-bearing rats resulted in an amelioration of all the
changes observed as a result of tumor burden. Administration
of this B
2
-adrenergic agonist also resulted in a decrease in
mRNAcontentofmusclePPARA,PPARD,andPPAR;,aswellas
inmRNAlevelsofmanyofthegenesinvolvedinbothlipidand
mitochondrial metabolism. All these results suggest an
involvement of the different PPARs as transcription factors
related with muscle wasting and also indicate that a possible
modeofactionoftheanticachecticcompoundformoterolmay
involve a normalization of the levels of these transcription
factors. [Cancer Res 2007;67(13):6512–9]
Introduction
Muscle wasting is a common feature in many pathologic states,
including infection and cancer (1). Muscle wasting, the main trend
of cachexia, is responsible for the death of at least 30% of cancer
patients (2). Although we know the main events related with
muscle wasting [activation of myofibrillar protein degradation,
induction of apoptosis, and activation of uncoupling proteins
(UCP); refs. 3, 4], we have contradictory evidence about the possible
mediators involved. Indeed, whereas involvement of different
cytokines, mainly tumor necrosis factor-a (TNFa) and interleu-
kin-6 (IL-6), has been postulated, other studies describe a more
direct role for tumor-derived factors, such as proteolysis-inducing
factor (PIF) and lipid-mobilizing factor (5, 6). The intracellular
signaling pathway may have a key role, from a therapeutic point of
view, especially if there are different mediators involved. Taking
this into consideration, a lack of knowledge about signaling
pathways and transcription factors involved in muscle wasting
exists. Some work has postulated a role for nuclear factor-nB
(NF-nB) in muscle wasting associated with cytokines (7) and
tumor-derived factors (8). Other transcription factors, such as
activator protein-1 (AP-1) and CCAAT/enhancer binding protein
(C/EBP), have also been involved in sepsis-induced muscle
cachexia (9). Results from our laboratory indicate that the
transcription factor AP-1 could also be involved during cancer
cachexia (10, 11). Not much attention has been focused on the role
of peroxisome proliferator-activated receptors (PPAR) in skeletal
muscle. These transcription factors are associated with changes in
lipid metabolism as well as UCP expression (12) and apoptosis (13).
PPARs are transcription factors belonging to the superfamily of
nuclear receptors. Three isoforms (a, y, and g) have been described
(14). They act on DNA response elements as heterodimers with the
nuclear retinoic acid receptor. Their natural activating ligands are
fatty acids and lipid-derived substrates. PPARa is present in liver,
heart, and, to a lesser extent, skeletal muscle; when activated, it
promotes fatty acid oxidation, ketone body synthesis, and glucose
sparing. PPARg is expressed in adipose tissue, lower intestine,
skeletal muscle, and immune cells; activation of PPARg induces the
differentiation of preadipocytes into adipocytes and stimulates
triglyceride storage. The PPARs are thus major regulators of lipid
and glucose metabolism, allowing adaptation to the prevailing
nutritional environment (14). PPARy has a broad expression
pattern in adult and is expressed very early during embryogenesis
(15). These past few years, it has been shown that treatment with
PPARy agonists normalizes blood lipids and also reduces insulin
resistance and adiposity in rodents and primates. Utilization of
both cellular and animal models revealed that this nuclear receptor
plays a central role in the control of fatty acid burning in adipose
tissue and skeletal muscle. Furthermore, PPARy seemed to be
important for adaptive response of skeletal muscle to environ-
mental changes, such as physical exercise (15).
h
2
-adrenergic agonists are potent muscle growth promoters in
many animal species (16, 17), resulting in skeletal muscle
hypertrophy (18–20) and reducing body fat content (21, 22).
Interestingly, results from our laboratory clearly indicate that
formoterol is a very efficient agent preventing muscle weight loss in
tumor-bearing rats (23). In vivo treatment can effectively reverse
muscle wasting loss decreasing protein degradation and increasing
the rate of protein synthesis in skeletal muscle, therefore favoring
protein accretion (23).
Bearing this in mind, the aim of the present investigation was to
ascertain if tumor burden induces any changes in PPARs gene
transcription in skeletal muscle and if these changes are associated
Requests for reprints: Josep M. Argile ´s, Cancer Research Group, Departament de
Bioquı ´mica i Biologia Molecular, Facultat de Biologia, Universitat de Barcelona,
Diagonal 645, 08028 Barcelona, Spain. Phone: 34-934021002; Fax: 34-934021559;
E-mail: jargiles@ub.edu.
I2007 American Association for Cancer Research.
doi:10.1158/0008-5472.CAN-07-0231
Cancer Res 2007; 67: (13). July 1, 2007 6512 www.aacrjournals.org
Research Article
Research.
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