632
Thromb Haemost 2002; 88: 632 – 8 © 2002 Schattauer GmbH, Stuttgart
Protein C Deficiency caused by Homozygosity for a Novel
PROC D180G Mutation – in vitro Expression and Structural
Analysis of the Mutation
Bent Lind
1
, Tobias Gedde-Dahl
2
, Geir Tjønnfjord
2
, Bruno O. Villoutreix
3
,
Frank Brosstad
4
1
Department of Clinical Biochemistry KB 3-01-1, Rigshospitalet, Copenhagen, Denmark
2
Medical Department A and
4
Research Institute for Internal Medicine, Rikshospitalet Oslo, Norway
3
INSERM U428, University of Paris V, School of Pharmacy, Paris, France
Keywords
Protein C deficiency, mutation, venous thrombosis, skin necrosis,
serine proteinase
Summary
Homozygosity for a novel D180G mutation in the protease domain
of protein C, associated with plasma protein C activity and antigen
levels of 8% of normal was identified in a thrombosis prone family.
Transient expression of protein C in HK-293 cells and analysis of
protein C antigen in culture media and cell lysates showed that the
secretion of mutant protein as compared with wild-type protein was
reduced by 79% while the intracellular contents were similar.
Computer analysis of the X-ray structure of activated protein C and
of a theoretical model of the zymogen predicts that the mutation
destabilises the molecule locally. Our results are compatible with a
relatively unstable mutant molecule that could be trapped inside the cell
and degraded. However, if secreted the mutant molecule could have a
relatively normal catalytic activity and structure consistent with the
plasma levels of protein C activity and the late onset of thrombosis.
Introduction
The vitamin K-dependent plasma glycoprotein protein C is the
precursor of the anticoagulant serine proteinase activated protein C that
plays a role in regulating blood coagulation (1, 2). Activated protein C
exerts its anticoagulant function by proteolytic inactivation of the blood
coagulation cofactors V
a
and VIII
a
in the presence of protein S and of
negatively charged membrane surface. Protein C (419 amino acid
residues) is produced mostly in the liver as a single-chain inactive
zymogen, which is proteolytically processed (removal of K156 and
R157) to a two-chain molecule composed of a light and a heavy chain
covalently bound through a disulphide bond (1). The light chain
(residues 1 through 155) is organised in several structural domains.
From the NH
2
-terminus to the C-terminus, they are the Gla-domain and
two epidermal growth factor modules (EGF). The heavy chain
(residues 170 to 419) consists of the serine proteinase domain. Under
physiological conditions, activated protein C is generated after a
specific proteolytic cleavage within its activation peptide by thrombin
(between R169 and L170), preferentially when the latter is bound to
thrombomodulin. Upon activation, the 12 amino acid activation
peptide of protein C is released (residues 158 to 169).
Protein C deficiency is an autosomally inherited disorder associated
with an increased risk of venous thrombosis (1, 2). Homozygosity and
compound heterozygosity for protein C deficiency is a rare condition
(prevalence about 1 in 200,000-400,000 individuals). In patients with
undetectable levels of protein C activity in plasma, massive thrombotic
complications may occur during the neonatal period. In patients with
very low but detectable levels of protein C activity in plasma the
clinical manifestations are milder and include late onset of thrombotic
symptoms and repeated episodes of skin necrosis. Heterozygosity for
protein C deficiency is characterised by an increased risk of venous
thrombosis in early adulthood. Anticoagulant treatment of protein C
deficient individuals with vitamin K antagonists (warfarin, coumarin,
phenprocoumon) may be complicated by warfarin-induced skin
necrosis (3).
In hereditary protein C deficiency more than 160 different mutations
have been reported (4). The mutations responsible for homozygote and
compound heterozygote protein C deficiency have been identified in 30
and 23 index patients, respectively (4 -16). In agreement with the
distribution of mutation types in genetic diseases in general (17) more
than 65% of the mutations identified in the protein C gene are missense
mutations. In most cases, their influence on the biosynthesis and
structure of protein C has not been studied.
The present work describes homozygosity for a novel D180G
mutation (D26 in the chymotrypsinogen nomenclature) in the protein C
gene associated with protein C deficiency, late onset of recurrent
venous thrombosis and recurrent warfarin induced skin necrosis. The
influence of the mutation on the biosynthesis of protein C was studied
in vitro in a transient expression system using human kidney (HK) 293
cells. Structural analysis of the activated protein C X-ray structure and
of a theoretical model for the protein C zymogen was also performed
to evaluate further the potential roles of the identified amino acid
substitution on folding and stability of the mutant protein C.
Materials and Methods
Clinical Material
Subjects under study were the proband, her parents and her 4 siblings
(Table 1). The study was performed after informed consent.
Correspondence to: Dr. Bent Lind, Department of Clinical Biochemistry
KB 3-01-1, Rigshospitalet, Blegdamsvej 9, DK-2100 Copenhagen, Denmark –
Tel.: + 45 35 45 30 11; Fax: + 45 35 45 25 24; E-mail: bli@kpll.dk
For personal or educational use only. No other uses without permission. All rights reserved.
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