© 2008 Schattauer GmbH, Stuttgart
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Immune complex-mediated glomerulonephritis is ameliorated
by thrombin-activatable fibrinolysis inhibitor deficiency
Nelson E. Bruno
1
, Yutaka Yano
1
, Yoshiyuki Takei
3
, Liqiang Qin
4
,Toshinari Suzuki
1
, John Morser
4,7
,
Corina N. D’Alessandro-Gabazza
2
, Akira Mizoguchi
6
, Koji Suzuki
5
, OsamuTaguchi
2
, Esteban C. Gabazza
4
,
Yasuhiro Sumida
1
1
Department of Diabetes and Endocrinology,
2
Department of Pulmonary and CriticalCare Medicine,
3
Department
of Gastroenterology and Hepatology,
4
Department of Immunology,
5
Department of Molecular Pathobiology,
6
Department of Neural
Regeneration and Cell Communication, Mie University Graduate School of Medicine,Tsu-city, Mie, Japan;
7
Department of Cardiovascular
Research, Berlex Biosciences, Richmond, California, USA
Summary
The activity of plasmin plays a critical role in the development of
chronic glomerulonephritis.Thrombin-activatable fibrinolysis in-
hibitor (TAFI) is a potent inhibitor of plasmin generation.We hy-
pothesized thatTAFI is involved in the pathogenesis of glomeru-
lonephritis because it inhibits plasmin generation.To demon-
strate this hypothesis, we compared the development of im-
mune complex-mediated glomerulonephritis in wild-type and
TAFI-deficient mice. After six weeks of treatment with horse
spleen apoferritin and lipoplysaccharide to induce glomerulo-
nephritis, mice deficient in TAFI had significantly better renal
function as shown by lower concentrations of albumin in urine
and blood urea nitrogen compared to wild-type mice. In addi-
Keywords
Knockout mouse, glomerulonephritis, coagulation, fibrin, cyto-
kines, plasmin, inflammation
tion, the activity of plasmin and matrix metalloproteinases was
significantly increased, and mesangial matrix expansion and the
deposition of collagen and fibrin in kidney tissues were signifi-
cantly decreased inTAFI-knockout mice as compared to their
wild-type counterparts. Depletion of fibrinogen by batroxobin
(Defibrase) treatment led to equalization of the renal function
and the amount of collagen deposition in the kidneys of TAFI-
knockout and wild-type mice with immune complex-mediated
glomerulonephritis. Together these observations suggest that
TAFI-mediated inhibition of plasmin generation plays a role in
the pathogenesis of glomerulonephritis, and that it may consti-
tute a novel molecular target for the therapy of this disease.
Thromb Haemost 2008; 100: 90–100
Wound Healing and Inflammation / Infection
Correspondence to:
Esteban C. Gabazza, MD, PhD
Department of Immunology, Mie University Graduate School of Medicine
Edobashi 2–174, Tsu-city, 514–8507 Mie, Japan
Tel.: +81 59 231 3180, Fax: +81 59 231 3180
E-mail: gabazza@clin.medic.mie-u.ac.jp
Financial support
The present investigation was supported by Grants-in-Aid (nos. 18590846, 17590788)
from the Ministry of Education, Culture, Sports, Science andTechnology of Japan, and by
Grants-in-Aids from the Mie Medical Research (2006), Okasan-Kato Foundation (2007)
and Suzuken Memorial (2005) Foundations, and the Mie University COE Project Fund.
Received February 18, 2008
Accepted after major revision May 20, 2008
Prepublished online June 11, 2008
doi:10.1160/TH08-02-0092
Introduction
The deposition of immune complex in the kidneys is a frequent
cause of chronic glomerulonephritis and subsequent renal fail-
ure (1). The presence of immune complexes in the glomerular
structures causes renal cell injury by activating the complement
system, by stimulating the infiltration of inflammatory cells and
by inducing the secretion of vasoactive substances, adhesion
molecules, cytokines and pro-coagulant factors from resident
cells (1–2). This initial inflammatory response may ultimately
evolve to an end-stage renal fibrosis, which is characterized by
increased accumulation of myofibroblasts, excessive deposition
of extracellular matrix proteins (e.g. collagen), progressive des-
truction of glomeruli and renal failure (3–4). Glomerulonephri-
tis caused by immune complex in humans are serum sickness
disease and autoimmune diseases such as systemic lupus erythe-
matosus, subacute bacterial endocarditis and hepatitis C-related
cryoglobulinemia (1).The mechanistic pathways involved in the
transition from tissue injury to fibrosis in the kidneys are not
understood but decreased local activation of extracellular ma-
trix-degrading enzymes may play a critical role (5–7). An impor-
tant physiological activator of matrix degradation in the kidneys
is the plasminogen-plasmin system (8–9). A balance between the
processes of degradation and deposition of extracellular matrix
is a fundamental requisite for maintaining the structural and
functional integrity of the glomerulus (5). Thus, decreased activ-
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