LETTERS
358 VOLUME 19 | NUMBER 3 | MARCH 2013 NATURE MEDICINE
Hepatic insulin resistance is a driving force in the pathogenesis
of type 2 diabetes mellitus (T2DM) and is tightly coupled with
excessive storage of fat and the ensuing inflammation within
the liver
1–3
. There is compelling evidence that activation of the
transcription factor nuclear factor-kB (NF-kB) and downstream
inflammatory signaling pathways systemically and in the liver
are key events in the etiology of hepatic insulin resistance and
b-cell dysfunction, although the molecular mechanisms involved
are incompletely understood
3–6
. We here test the hypothesis
that receptor activator of NF-kB ligand (RANKL), a prototypic
activator of NF-kB, contributes to this process using both an
epidemiological and experimental approach. In the prospective
population-based Bruneck Study, a high serum concentration
of soluble RANKL emerged as a significant (P < 0.001) and
independent risk predictor of T2DM manifestation. In close
agreement, systemic or hepatic blockage of RANKL signaling
in genetic and nutritional mouse models of T2DM resulted in a
marked improvement of hepatic insulin sensitivity and amelioration
or even normalization of plasma glucose concentrations and
glucose tolerance. Overall, this study provides evidence for a role of
RANKL signaling in the pathogenesis of T2DM. If so, translation to
the clinic may be feasible given current pharmacological strategies
to lower RANKL activity to treat osteoporosis.
RANKL (also known as TNFSF11) is a member of the tumor necrosis
factor superfamily and, after ligation with its cognate receptor RANK
(also known as TNFRSF11a), is a potent stimulator of NF-κB. Notably,
both RANKL and RANK are expressed in human liver tissue and
pancreatic β-cells
7
, and concentrations of the soluble decoy receptor
osteoprotegerin (OPG), considered to be a reliable surrogate for the
overall activity of this cytokine network, are elevated in patients with
T2DM, especially in those with poor glycemic control and compli-
cated disease course
8–11
. RANKL exists in both membrane-bound
and biologically active soluble forms, with the latter originating from
secretion and cleavage
9,12
. Concentrations of soluble RANKL are ele-
vated in or predictive of various human diseases, including cardiovas-
cular disease, nontraumatic fractures, multiple myeloma, rheumatoid
arthritis and inflammatory bowel disease
8–11,13–18
. We determined
the distribution of serum concentrations of RANKL and OPG in our
study population (n = 844) (Supplementary Fig. 1a). Soluble RANKL
concentrations showed associations with insulin resistance assessed
by homeostasis model (HOMA-IR) and Gutt Index values and with
the number of metabolic syndrome components clustering in an indi-
vidual (Supplementary Data) but were not related to most standard
population characteristics (Supplementary Table 1).
Between 1990 and 2005, 78 of the 844 individuals in the study
population (9.2%) developed T2DM (incidence rate, 7.2 per 1,000
person years (95% confidence interval (CI) 5.7–8.9)). We determined
the baseline characteristics of subjects with and without incident
T2DM (Supplementary Table 2) and found that the concentrations
of soluble RANKL differed considerably between the two groups. In
a pooled logistic regression analysis adjusted for age, sex and period
Blockade of receptor activator of nuclear factor-κB
(RANKL) signaling improves hepatic insulin resistance
and prevents development of diabetes mellitus
Stefan Kiechl
1,16
, Jürgen Wittmann
2
, Andrea Giaccari
3,4
, Michael Knoflach
1
, Peter Willeit
1,5
, Aline Bozec
6
,
Alexander R Moschen
7
, Giovanna Muscogiuri
3
, Gian Pio Sorice
3
, Trayana Kireva
6
, Monika Summerer
8
,
Stefan Wirtz
9
, Julia Luther
6
, Dirk Mielenz
2
, Ulrike Billmeier
9
, Georg Egger
10
, Agnes Mayr
11
,
Friedrich Oberhollenzer
10
, Florian Kronenberg
8
, Michael Orthofer
12
, Josef M Penninger
12
, James B Meigs
13,14
,
Enzo Bonora
15
, Herbert Tilg
7
, Johann Willeit
1
& Georg Schett
6,16
1
Department of Neurology, Medical University Innsbruck, Innsbruck, Austria.
2
Department of Internal Medicine 3, Division of Molecular Immunology, University of
Erlangen-Nuremberg, Erlangen, Germany.
3
Division of Endocrinology and Metabolic Diseases, Università Cattolica del Sacro Cuore, Policlinico ‘A. Gemelli’, Rome,
Italy.
4
Fondazione Don Gnocchi, Milan, Italy.
5
Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
6
Department of Internal
Medicine 3, University of Erlangen-Nuremberg, Erlangen, Germany.
7
Department of Medicine I, Division of Endocrinology, Gastroenterology and Metabolism,
Medical University Innsbruck, Innsbruck, Austria.
8
Department of Medical Genetics, Division of Genetic Epidemiology, Molecular and Clinical Pharmacology,
Medical University Innsbruck, Innsbruck Austria.
9
Department of Internal Medicine I, University of Erlangen-Nuremberg, Erlangen, Germany.
10
Department of
Internal Medicine, Bruneck Hospital, Bruneck, Italy.
11
Department of Laboratory Medicine, Bruneck Hospital, Bruneck, Italy.
12
Institute of Molecular Biotechnology
of the Austrian Academy of Sciences (IMBA), Vienna, Austria.
13
Department of Internal Medicine, Harvard University, Boston, Massachusetts, USA.
14
Department of
Medicine, General Medicine Division, Massachusetts General Hospital, Boston, Massachusetts, USA.
15
Division of Endocrinology, Diabetes and Metabolic
Diseases, University and Hospital Trust of Verona, Verona, Italy.
16
These authors contributed equally to this work. Correspondence should be addressed to
S.K. (stefan.kiechl@i-med.ac.at) or G.S. (georg.schett@uk-erlangen.de).
Received 25 October 2012; accepted 8 January 2013; published online 10 February 2013; doi:10.1038/nm.3084
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