Psoriasis-associated vascular disease: the role of HDL
Paiva-Lopes and Delgado Alves Journal of Biomedical Science
Psoriasis-associated vascular disease: the role of HDL
Maria Joao Paiva-Lopes 0 1 4
José Delgado Alves 0 3
0 CEDOC, NOVA Medical School
1 Serviço de Dermatologia, Hospital dos Capuchos CHLC, Alameda de Santo António dos Capuchos , 1169-050 Lisboa , Portugal
2 Faculdade de Ciências Médicas, Universidade NOVA de Lisboa , Campo dos Mártires da Pátria, 130, 1169-056 Lisboa , Portugal
3 Immunomediated Systemic Diseases Unit (UDIMS), Fernando Fonseca Hospital , Amadora , Portugal
4 Serviço de Dermatologia, Hospital dos Capuchos CHLC, Alameda de Santo António dos Capuchos , 1169-050 Lisboa , Portugal
5 Faculdade de Ciências Médicas, Universidade NOVA de Lisboa , Campo dos Mártires da Pátria, 130, 1169-056 Lisboa , Portugal
Psoriasis is a chronic inflammatory systemic disease with a prevalence of 2-3%. Overwhelming evidence show an epidemiological association between psoriasis, cardiovascular disease and atherosclerosis. Cardiovascular disease is the most frequent cause of death in patients with severe psoriasis. Several cardiovascular disease classical risk factors are also increased in psoriasis but the psoriasis-associated risk persists after adjusting for other risk factors. Investigation has focused on finding explanations for these epidemiological data. Several studies have demonstrated significant lipid metabolism and HDL composition and function alterations in psoriatic patients. Altered HDL function is clearly one of the mechanisms involved, as these particles are of the utmost importance in atherosclerosis defense. Recent data indicate that biologic therapy can reverse both structural and functional HDL alterations in psoriasis, reinforcing their therapeutic potential.
Psoriasis; Atherosclerosis; High-density lipoproteins (HDL); HDL function; Anti-HDL antibodies
Psoriasis is an immunomediated disease classified by
some authors as autoimmune [
], although the nature
of the antigens involved is still unknown. It is the most
prevalent chronic inflammatory disease in humans, with
an estimated global prevalence of 2–3% .
Erythematous plaques covered by silvery scales characterize it
clinically. Pathology shows keratinocyte hyperplasia and
an inflammatory infiltrate. Psoriatic arthritis has been
recognized as a comorbidity for many years but only
recently has the association with other comorbidities
been identified and studied [
]. Psoriasis patients have a
higher prevalence of cardiovascular disease (CVD) and
associated risk factors, including dyslipidaemia, higher
blood pressure and higher body mass index, as
demonstrated in a meta-analysis comprising 59 studies with up
to 18,666 cases and 50,724 controls [
psoriasis is an independent risk factor for CVD even
after controlling for traditional risk factors.
Cardiovascular disease is associated with a 6-year
shorter life expectancy in patients with severe psoriasis
]. According to a meta-analysis of 14 studies, the risk
for cardiovascular mortality was 1.37, the risk for
myocardial infarction was 3.04 and the risk for stroke 1.59
times higher in patients with severe psoriasis than in the
general population [
Atherosclerosis is the pathological process underlying
cardiovascular disease (CVD) and mortality. All phases
of atherosclerosis are related to inflammatory events, in
a strikingly similar fashion to the inflammatory events
observed in psoriasis [
]. Furthermore, these two diseases
share common immunologic pathways involving dendritic
cells, Th1, Th17 and Treg cells as well as several angiogenic
factors and oxidative mechanisms [
]. Not surprisingly,
psoriasis has been demonstrated to be an independent risk
factor for subclinical atherosclerosis [
High-density lipoproteins (HDL) are of pivotal importance
in atherosclerosis. These are extremely complex
particles with a unique capacity for milieu adaptation,
constantly changing both its chemical composition and its
tri-dimensional structure [
]. HDL has anti-oxidative,
anti-inflammatory, anti-apoptotic and anti-thrombotic
] hence its importance goes much beyond
reverse cholesterol transport. These functions depend
more on HDL quality and function than on HDL–C
This review discusses psoriasis-associated alterations
in HDL structure and function that may play a role in
atherogenesis and vascular disease associated with
psoriasis. We searched ISI Web of Science, Medline and
PubMed for psoriasis, atherosclerosis, cardiovascular
disease, HDL, dysfunctional HDL and anti-HDL
antibodies. We started by searching for each term separately
and afterwards an advanced search was carried out by
combining “psoriasis” with each search term in
keywords, abstracts and/or titles. The references cited in
the selected articles were also analysed. After a
comprehensive review, duplications were excluded and the final
selection was based on relevance and date.
Lipid metabolism in psoriasis
Lipid metabolism in patients with psoriasis has been a
subject of study for more than 50 years. Numerous studies
show decreased levels of HDL and/or increased levels of
low-density lipoproteins (LDL) and of very-low density
lipoproteins (VLDL) and triglycerides (TG) [
However, some studies failed to demonstrate an association
between lipid serum levels and psoriasis [
including a large population-based cross-sectional study in the
UK . In this study, psoriatic patients had
hyperlipidaemia (odds ratio 1.16) but the results were not significant
when controlled for obesity and diabetes, which can also
The published studies are heterogeneous because they
include patients with different disease durations and
systemic treatments, factors that may per se influence
the lipid metabolism. Based on the results of 200
patients investigated at the onset of skin disease showing
higher cholesterol concentrations in VLDL and HDL,
Mallbris et al. [
] suggested that lipid abnormalities in
psoriasis could be genetically determined rather than a
consequence of the psoriasis pathogenic events and
treatments on the lipoprotein phenotype. The lipid
disturbances associated with the immunologic abnormalities led
to the suggestion that psoriasis should be regarded as an
immunometabolic disease [
HDL composition and function
Lipoproteins form a complex lipid transport system. The
smallest lipoproteins in molecular size are HDL and they
contain the highest proportion of apolipoproteins to
lipids. Apolipoprotein A-I (apoA-I) and apolipoprotein
A-II (apoA-II) are major HDL associated proteins. They
are secreted into plasma by the liver and the intestine.
The highly dynamic and flexible conformation of the
apoA-I molecule provides a possible explanation for
how apoA-I determines HDL subclass structure and
12, 24, 25
HDL takes up cholesterol from cell membranes and
other lipoproteins and transports it from the periphery
to the liver for excretion during the process of reverse
cholesterol transport (RCT). Active export of excess
cholesterol to HDL is mediated by the ATP-binding
cassette transporters ABCA1 and ABCG1/G4. RCT is a
process of major biological importance and is believed
to be an important mechanism to explain how HDL
might prevent cardiovascular disease.
Furthermore, HDL has several anti-inflammatory and
antioxidant functions that may also be as important as
RCT in protecting against atherosclerosis (Table 1).
Noticeably, HDL has antioxidant properties, attributable
mostly to apoA and paraoxonase (PON-1), and inhibits
oxidative modifications of LDL. HDL also inhibits
monocyte transmigration as well as the expression of
adhesion molecules in endothelial cells. These properties
seem to be independent from RCT [
Apolipoprotein E (apoE) is another important
component of the HDL particle [
]. It is a polymorphic
multifunctional protein recognized for its remarkable capacity
to suppress atherosclerosis. Animal models show a
nonlipid antiatherogenic effect of apoE, possibly explained
by its antioxidant, antiproliferative (smooth muscle cells
and lymphocytes), anti-inflammatory, antiplatelet, and
nitric oxide (NO)–generating properties [
Furthermore, apoE suppresses nuclear factor-κB mediated
HDL high-density lipoproteins, ABCA1 ATP-binding cassette transporter A1,
ABCG1 ATP-binding cassette transporter G1, SR-BI scavenger receptor class B
type I, VCAM-1 vascular cell adhesion molecule-1, LDL low-density lipoprotein,
ox-LDL oxidized LDL, ROS reactive oxygen species, NO nitric oxide, eNOS
endothelial nitric oxide synthase
inflammation in monocytes and macrophages, thus
supressing atherosclerosis [
]. ApoE is also involved in
cellular signalling and it may control macrophage
plasticity and endothelial cell activation. Inflammatory
cytokines can upregulate or downregulate the
production of apoE in various tissue types and the cross-talk
between apoE and cytokines has an important role in
several disorders [
ApoE polymorphisms modulate susceptibility to many
diseases, namely neurodegenerative disorders and
atherosclerosis, as well as psoriasis [
]. In a meta-analysis
involving seven studies with 966 patients and 1086
controls, results indicate that the allele ε4 may influence
psoriasis severity in Europeans, the allele ε2 is associated
with increased susceptibility for psoriasis and the allele ε3
may decrease psoriasis risk . These results must be
interpreted with caution since the allelic distribution of
apoE varies worldwide and the number of studies in the
literature is small and involves only Europeans and Asians.
Alleles ε2 and ε4 are also associated with increased
cardiovascular risk [
Whilst most studies have been focused on the HDL
protein components, the HDL lipids represent 50–80%
of the total HDL mass and have been shown to affect
particle stability, cholesterol efflux from macrophages
and cholesterol elimination [
]. It is now recognized
that lipid composition, namely phospholipids also play
an essential role on HDL functionality [
HDL and chronic inflammation
HDL has known immunomodulating properties related
both to the innate and the adaptive immune system [
HDL modulates several immune cell functions, mainly
by modifying the lipid rafts’ cholesterol content. Thereby
it modulates dendritic cells (DC), monocytes,
macrophages, T cells and B cells [
]. Importantly, apoA-1
stimulates production of IL-10 and PGE2, thus inhibiting
DC differentiation and function [
] and decreasing T cell
activation and IL-12 production [
]. HDL protects from
oxidative damage by terminating chain reactions of lipid
peroxidation. Several apolipoproteins (apoA-I, apoA-II,
apoA-IV, apoA-V, apoE, apoJ, apoM) and enzymes
(PON1, LCAT, platelet activating factor-acetyl hydrolase)
contribute to this effect [
In chronic inflammatory diseases however, the
antioxidative and anti-inflammatory properties of HDL become
]. Proteome alterations, which include
decreased activity of HDL-associated enzymes and
accumulation of complement (C3), ceruloplasmin and
SAA, result in loss of the antioxidant capacity of HDL.
Impaired cellular efflux of lipids to HDL is another
pro-inflammatory mechanism that is associated with
activation of intracellular STAT3 signalling and
enhanced vascular inflammation [
These phenomena are important in chronic inflammatory
diseases like rheumatoid arthritis and systemic lupus
erythematosus (SLE), which are also associated with increased
risk of cardiovascular disease. Chronic inflammation
induced alterations in lipid metabolism certainly contribute
to the higher atherosclerotic risk in these patients.
In patients with psoriasis, not only lipoprotein levels
can be altered, but also their composition and function
may be significantly different from controls. This is an
important observation because the composition and
function of HDL are actually considered more important
than the quantity of HDL itself.
Mehta et al. [
] found a more atherogenic lipoprotein
profile and decreased HDL efflux capacity in 112
psoriasis patients when compared to controls. In this study,
nuclear magnetic resonance showed an atherogenic
profile in psoriasis similar to that observed in diabetes,
with significant increase in LDL particle concentration
and decrease in LDL size. Also HDL efflux capacity was
lower in psoriasis compared to controls.
HDL isolated from 15 psoriatic patients [
significant differences in the HDL-associated proteins:
reduction of apoA-1 and apo-M and higher levels of
acute-phase proteins such as serum amyloid A (SAA),
prothrombin, α-1-antitrypsin and α-1-acid glycoprotein
1. The lipid composition of HDL was also altered in
these patients; a decrease in the phospholipid and
cholesterol content of HDL was observed. Additionally, this
study showed a diminished cholesterol efflux capability
that correlated with loss of apoA-1, phosphatidylcholine
and sphingomyelin in HDL from psoriatic patients.
However, Holzer reported no modification of HDL
antioxidative activity, assessed by the capacity to inhibit
A recent study demonstrated that psoriasis associated
HDL particle characteristics and function were also
altered in 44 paediatric patients with psoriasis. These
patients showed reduced cholesterol efflux capacity
compared to age-matched controls, before and after
adjusting for confounding variables, suggesting that
reverse cholesterol transport defects start early in life
even with low levels of chronic inflammation [
A cross-sectional study designed to characterize the
biologic activities of plasma lipoproteins, involving 25
patients with psoriasis and 25 controls, showed lower
plasma levels of HDL and reduced PON-1 activity.
PON-1 activity was found to negatively correlate to
disease severity, measured by PASI. Other HDL
properties were also altered, namely a) protection against LDL
oxidation, b) inhibition of TNF-α induced monocyte
adherence to endothelial cells, c) prevention of oxidized
low-density lipoprotein (ox-LDL)-induced monocyte
migration and d) protection of endothelial cells from
TNF-α induced apoptosis [
Tom (43): 44 paediatric patients Reduced cholesterol efflux capacity
HDL high-density lipoprotein, apoA-I apolipoprotein A-I, apo-A-II apolipoprotein
A-II, apoM apolipoprotein M, SAA serum amyloid A, PON-1 paraoxonase 1
The authors declare that they have no competing interests.
Reduced PON-1 activity was also demonstrated by Usta
] in a cohort of 25 patients and Ferreti in a study of 23
]. However, this results were unconfirmed by
other studies which found an increased [
] or not altered
] PON activity. Interestingly, PON1 55 M allele is a risk
factor for psoriasis: a case-control study of 100 patients
with psoriasis demonstrated an association of this allele
with an impairment of the antioxidant system and an
abnormal lipid metabolism [
In chronic inflammatory conditions, protein structural
modification and appearance of neo-epitopes may lead to
autoantibody production and further HDL dysfunction.
Elevated titres of autoantibodies against HDL (aHDL)
and apoA-I have been demonstrated in diseases
associated with an increased cardiovascular risk [
These antibodies have been recognized as a new
biomarker for vascular disease in the context of autoimmune
]. We have recently demonstrated the
presence of aHDL and aApo A-I antibodies in patients with
psoriasis. These antibodies were associated with increased
disease severity and may contribute to the pathogenesis of
atherosclerosis in this condition [
It should be emphasized that published studies are
heterogeneous regarding both clinical and laboratorial
data. Patient selection includes different types of psoriasis
(e.g. with or without arthritis) in various clinical stages
with varying degrees of inflammation or remission and
under different systemic therapies. Laboratory
methodology is also variable; measuring HDL-cholesterol is not
equivalent to measuring HDL particle number. NMR
spectroscopy and ion mobility can be used to quantify
HDL particles, however, these methods give different
estimates of HDL particle concentration and size. Another
problem is that all methods used to assess HDL subclasses
measure only static concentrations with no assessment of
the dynamic processes regulating HDL subclasses [
Despite these difficulties, the studies clearly show that
psoriasis alters both the proteomic and lipid composition
of HDL and these changes result in decreased cholesterol
efflux capacity and reduced anti-inflammatory and
antioxidant properties of HDL (Table 2). Furthermore,
these findings have been corroborated by the observation
that anti-psoriatic therapy, both conventional (specially
systemic) and biologic, recovers HDL composition and
]. Noticeably, treatment with anti-TNF-α
was associated with amelioration of myocardial
dysfunction . These studies suggest that adequate treatment,
especially with biologic agents, can improve psoriasis
patients’ cardiovascular risk.
Inflammatory processes occurring chronically in psoriasis
have an impact on HDL in many different ways resulting
in proteomic and lipid composition alterations and
consequently altered HDL function. These alterations help to
explain the epidemiological evidence associating psoriasis
to atherosclerosis and CVD, though further investigation
on this subject is necessary. Importantly, anti-psoriatic
therapy reverses these alterations. A better understanding
of these mechanisms of disease will contribute to the
development of novel biomarkers and of new therapeutic
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MPL contributed to the concept, writing and reviewing, JDA contributed to
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manuscript. Both authors have contributed significantly and are in
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