1 3
Arch Toxicol
DOI 10.1007/s00204-016-1830-8
ORGAN TOXICITY AND MECHANISMS
TLR4-mediated inflammation is a key pathogenic event leading
to kidney damage and fibrosis in cyclosporine nephrotoxicity
Cristian González-Guerrero
1,2
· Pablo Cannata-Ortiz
2,3
· Consuelo Guerri
4
·
Jesús Egido
1,5
· Alberto Ortiz
1,2,5
· Adrián M. Ramos
1,2,6
Received: 16 June 2016 / Accepted: 24 August 2016
© Springer-Verlag Berlin Heidelberg 2016
also reduced tubular damage and drastically prevented the
development of kidney fibrosis. In vivo and in vitro CsA
promoted secretion of the TLR ligand HMGB1 by tubu-
lar cells upstream of TLR4 activation, and prevention of
HMGB1 secretion significantly reduced CsA-induced
synthesis of MCP-1, suggesting that HMGB1 may be one
of the mediators of CsA-induced TLR4 activation. These
results suggest that TLR4 is a potential pharmacological
target in CsA nephrotoxicity.
Keywords Cyclosporine A · TLR4 · Innate immunity ·
Nephrotoxicity · Inflammation · Fibrosis
Introduction
Cyclosporine A (CsA) was the first calcineurin inhibi-
tor (CNI) available in the clinic and is still extensively
used throughout the world. In fact, CsA is the only CNI
included in the last updated World Health Organization
(WHO) list of essential medicines (WHO 2015). CsA
was a breakthrough that increased organ and patient sur-
vival. Moreover, CsA is routinely used to treat autoim-
mune disorders (Ponticelli 2005). Unfortunately, chronic
CsA therapy increases the risk of chronic nephrotoxicity
(Naesens et al. 2009). Although acute renal side effects
may be reversible and can be minimized through strate-
gies to reduce drug exposure, this often does not prevent
chronic nephrotoxicity, a subtle, non-reversible process
leading to progressive organ fibrosis (Sawinski et al. 2016).
Molecular mechanisms underlying CsA nephrotoxicity
have been extensively researched, although they remain to
be completely characterized. Inflammation encompasses
adaptive and protective mechanisms set in motion to repair
damaged tissues and eliminate invading microorganisms.
Abstract Cyclosporine A (CsA) successfully prevents
allograft rejection, but nephrotoxicity is still a dose-lim-
iting adverse effect. TLR4 activation promotes kidney
damage but whether this innate immunity receptor medi-
ates CsA nephrotoxicity is unknown. The in vivo role of
TLR4 during CsA nephrotoxicity was studied in mice co-
treated with CsA and the TLR4 inhibitor TAK242 and also
in TLR4
-/-
mice. CsA-induced renal TLR4 expression in
wild-type mice. Pharmacological or genetic targeting of
TLR4 reduced the activation of proinflammatory signaling,
including JNK/c-jun, JAK2/STAT3, IRE1α and NF-κB and
the expression of Fn14. Expression of proinflammatory fac-
tors and cytokines was also decreased, and kidney mono-
cyte and lymphocyte influx was prevented. TLR4 inhibition
Electronic supplementary material The online version of this
article (doi:10.1007/s00204-016-1830-8) contains supplementary
material, which is available to authorized users.
* Adrián M. Ramos
amramos@fjd.es
1
Laboratory of Nephrology and Vascular Pathology,
IIS-Fundación Jiménez Díaz, School of Medicine, Madrid,
Spain
2
REDINREN, Madrid, Spain
3
Pathology, IIS-Fundación Jiménez Díaz, School of Medicine,
UAM, Madrid, Spain
4
Department of Cellular Pathology, Centro de Investigación
Príncipe Felipe, Valencia, Spain
5
Fundación Renal Íñigo Álvarez de Toledo (FRIAT), Madrid,
Spain
6
Laboratorio de Patología Renal y Vascular (Investigación,
4° planta), Instituto de Investigación Sanitaria-Fundación
Jiménez Díaz, Av. Reyes Católicos N°2, CP28040 Madrid,
Spain