(VEGF) production in human monocyte/macrophages

Transkrypt

Magdalena Pertyńska-Marczewska1, 2, Serafim Kiriakidis1,
Robin Wait1, Jonathan Beech1, Katarzyna Cypryk2,
Marc Feldmann1, Ewa M. Paleolog1
PRACA ORYGINALNA
1
Kennedy Institute of Rheumatology, Faculty of Medicine, Imperial College, London, United Kingdom, 2Polish Mother's Memorial
Hospital Research Institute, Łódź, Poland
Advanced glycation end products (AGE) enhance
vascular endothelial growth factor (VEGF) production
in human monocyte/macrophages
Stymulacja końcowymi produktami glikacji (AGE) a wzrost produkcji czynnika wzrostu
śródbłonka (VEGF) w ludzkich komórkach monocytarnych
Streszczenie
Wstęp. W następstwie cukrzycy w licznych tkankach dochodzi do zwiększenia ekspresji czynników wzrostu naczyń
w odpowiedzi zarówno na hiperglikemię, jak i niedotlenienie
tkanek. Najważniejszym regulatorem procesów angiogenezy
jest czynnik wzrostu śródbłonka (VEGF). Końcowe produkty
glikacji białek (AGE) powstają w reakcji Maillarda i obecnie
uważa się je za współodpowiedzialne za rozwój powikłań
naczyniowych, zwłaszcza cukrzycy.
Cel. Określenie produkcji VEGF przez monocyty/makrofagi
stymulowane glikowanym białkiem ludzkim (HSA), powstałym w różnych procesach glikacji in vitro oraz przez białko
wołowe (BSA), modyfikowane przez Ne-(karboksymetyl)lizynę (CML-BSA).
Materiał i metody. Glikowane białko ludzkie inkubowano
z D-glukozą w buforze fosforanowym (PBS) lub w buforze
sodowo-fosforanowym w 37°C (150 mM) przez różny okres
czasu. Natomiast BSA inkubowano z cyjanobromowodor-
Background
The term advanced glycation end products (AGE) is
applied to a broad range of advanced products of reacAdres do korespondencji: dr hab. med. Katarzyna Cypryk
Klinika Endokrynologii ICZMP
Rzgowska 281/289, Łódź
tel. +48 (0 prefiks 42) 271 11 54
e-mail: [email protected]
Diabetologia Doświadczalna i Kliniczna 2003, 3, 6, 481–487
Copyright © 2003 Via Medica, ISSN 1643–3165
kiem sodu oraz kwasem glioksylowym w buforze fosforanowym w celu otrzymania białka wołowego modyfikowanego
Ne-(karboksymetyl)lizyną (CML- BSA).
Wyniki. Zaobserwowano silną stymulację produkcji VEGF
w nadsączach badanych komórek po stymulacji 600 mg/ml
glikowanym HSA w stężeniu (9 tygodni inkubacji z 1,67 M
glukozą) w NaH2PO4 w porównaniu ze stymulacją nieglikowanym HSA. Monocyty inkubowano przez okres od 4–24
godzin w obecności 1–9,5 mg/ml BSA modyfikowanego CML
oraz niemodyfikowanego BSA. Znamienny wzrost produkcji
VEGF zaobserwowano jedynie, stosując stężenie 9,5 mg/ml
BSA-CML.
Wnioski. Uzyskane wyniki sugerują, że AGE odgrywa bardzo ważną rolę w stymulacji rozwoju powikłań naczyniowych obserwowanych u chorych na cukrzycę.
słowa kluczowe: czynnik wzrostu śródbłonka (VEGF),
ludzkie makrofagi, powikłania naczyniowe cukrzycy
tion, such as N-(carboxymethyl)hydroxylysine, pyraline,
pentosidine, and cross-links. AGE are formed after glucose binds to protein amino residues and forms early
glycation products such as Schiff bases and Amadori
products. The final Maillard reaction leading to the production of AGE is slow, irreversible and dependent on
plasma glucose concentration. AGE are thus non-enzymatically glycated and autooxidized proteins [1]. Targets of advanced glycation include structural proteins,
such as collagen and aggrecan, plasma proteins, including immunoglobulins and albumin, and intracellular
www.ddk.viamedica.pl
481
Diabetologia Doświadczalna i Kliniczna rok 2003, tom 3, nr 6
proteins, such as haemoglobin and lens crystallin [2].
Protein glycation in particular has the potential to alter
many cellular functions, and as a consequence it has
been suggested that AGE contribute to the pathogenesis of many diseases. For example, Ne-(carboxymethyl)lysine (CML) and pentosidine products are elevated
in diabetes, and correlate with the severity of diabetic
microvascular disease [3]. Moreover, AGE-bovine serum albumin (BSA) has been shown to increase adhesion molecule expression on endothelial cells [4, 5].
Although the mechanisms leading to the vascular complications of diabetes are not fully understood, formation
and signalling through AGE is considered to be one of
such important mechanisms [6]. A link between AGE and
complications of diabetes is suggested by the observation that retinal, glomerular and nerve lesions induced by
experimental diabetes in animals are prevented by aminoguanidine, an inhibitor of AGE formation [7].
Angiogenesis is regulated by vascular growth factor,
particularly the vascular endothelial growth family of proteins (VEGF). Recently Ido and colleagues reported that
vascular dysfunction induced by AGE is mediated by
VEGF via mechanisms involving reactive oxygen species, guanylate cyclase, and protein kinase C [8]. AGE
have also been shown to increase VEGF release and to
stimulate the growth of microvascular endothelial cells,
which might contribute to diabetic microangiopathies
[8–11] and the amount of AGE has been reported to
correlate with the severity of diabetic complications [12].
In this report we aim to show that AGE-modified proteins stimulate human monocyte-derived macrophages
to produce VEGF. Our results suggest an important role
for AGE in the stimulation of the development of angiogenesis observed in diabetic complications.
incubation using Schleicher & Schuell filters with a cut
off equivalent of 0.2 mm. All buffers were prepared in
endotoxin-free H2O.
HSA (1 mM) was minimally modified by AGE by incubation with 50 mM D-glucose in PBS at 37°C for
5 weeks. HSA (1 mM) was extensively modified by AGE
by incubation with 1.67 M D-glucose in PBS at 37°C for
9 weeks. As controls, HSA was incubated without glucose in PBS for either 5 weeks or 9 weeks. Alternatively,
both highly and minimally modified HSA were prepared
in a 150 mM NaH2PO4 buffer of pH 7.4 as described
above. After incubation, proteins were dialyzed against
distilled water for 24 hours at 4°C to remove any unincorporated sugars [13].
Glycated BSA and HSA preparations were scanned
in a Perkin Elmer Spectrometer Lambda Bio 50. BSA
and HSA incubated in the absence of glucose were used
as controls. Additionally, mass spectrometry was carried out to characterize the primary structure of the samples (data not shown).
Synthesis of CML-modified albumin
To synthesise CML-modified albumin, BSA (176 mg/ml)
was dissolved in a 0.2 M NaH2PO4 buffer of pH 7.8,
containing 450 mM sodium cyanoborohydride [14].
Glyoxylic acid was added to this solution to give
a concentration of 155 mM, and the mixture was incubated for 24 hours at 37°C, before dialysis against
cold PBS for 48 hours at 4°C. Control proteins were
prepared under the same conditions, except that
glyoxylic acid was omitted. The dialyzed CML-BSA
and BSA control solutions were filter-sterilized and aliquoted for storage at –80°C.
Isolation of monocyte/macrophages
Materials and methods
Reagents
Bovine serum albumin (fraction V, 96–99% albumin,
< 1 ng endotoxin/mg; BSA), b-D-glucose, human serum
albumin (fraction V, 96 to 99% albumin, HSA), polimyxin
B were purchased from Sigma (Poole, Dorset, UK).
Escherichia coli lipopolysaccharide (LPS) was obtained
from Sigma (St. Louis, USA). All reagents used to prepare AGE were of analytical grade.
Preparation of HSA-AGE
Glycated HSA was prepared under sterile conditions
in the dark and in the presence of protease inhibitors
(PMSF 1.5 mM, leupeptin 0.5 mg/ml, aprotinin 2 mg/ml,
pepstatin 0.1 mg/ml). Each sample was filtered prior to
482
Human monocytes were differentiated to macrophages, as described previously [15, 16]. Briefly, single-donor platelet pheresis residues were purchased
from North London Blood Transfusion Service (Colindale, UK). Mononuclear cells were isolated by Ficoll-Hypaque centrifugation prior to monocyte separation
in a Beckman Instruments JEL elutriator (Torrence,
CA, USA). Monocyte purity was assessed by flow cytometry and was routinely found to be > 90%. Elutriated human monocytes were incubated at 106/ml in
RPMI 1640 with 2 mM L-glutamine supplemented with
5% (v/v) heat-inactivated foetal calf serum (FCS) and
100 U/ml penicillin/streptomycin, together with macrophage colony-stimulating factor (M-CSF; 100 ng/ml;
from Genetics Institute, Boston, MA, USA) for 48 hours for differentiation to a macrophage-like phenotype. Adherent cells were washed twice in FCS-free
RPMI 1640 and removed using Cell Dissociation Medium (Sigma, Poole, UK).
Magdalena Pertyńska-Marczewska et al. AGE induces VEGF production in human macrophages
Monocyte/macrophages were plated at 105 cells per
30 mm2 well and stimulated with or without glycated
HSA or BSA, or with non-glycated product as a control.
Cells were also stimulated under the same conditions
with CML-modified BSA, or with unmodified BSA as
a control. Polymyxin B (2.5 mg/ml) was used in all experiments, and LPS (10 ng/ml) was used as a control stimulus. After 4–24 hours at 37°C and 5% CO2, the cells were
sedimented by centrifugation, the supernatants removed and assayed for cytokine release as described below. Alternatively, cells were lysed for measurement of
tissue factor antigen, as described below.
The addition of either minimally and extensively glycated HSA, or CML-BSA, was without effect on cell viability, monitored using MTT.
Analysis of cytokine release by ELISA
To assay VEGF production, polystyrene plates (Nunc-Immunoplate II, BRL, Middlesex, UK) were coated with
anti-human VEGF antibody (R&D, Abingdon, UK; 100 ng/ml
in PBS) overnight at 4°C. Recombinant human VEGF
standard (R&D, Abingdon, UK) or samples were added
overnight at 4°C. Biotinulated anti-human VEGF antibody (50 mg/ml in 0.5% BSA/PBS) was then added at room
temperature for 2 hours. Plates were washed to remove
the detection antibody and incubated for 1 hour with
streptavidin-horseradish peroxidase (HRP; Amersham
Life Sciences, Buckinghamshire, UK). After the removal
of the HRP conjugate, the plates were washed with PBS
containing 0.05% Tween 20, and a 1:1 mixture of H2O2
and 3, 3', 5, 5'-tetramethylbenzidine peroxidase substrate (Kirkegaard and Perry Laboratories, Gaithersburg,
MD, USA) was added for 5 minutes. After addition of 2 M
sulphuric acid, plates were read at 450 nm on a spectrophotometric ELISA plate reader (Labsystems Multiscan Biochromic) and analysed using a Delta Soft II-4
program.
Statistical analysis
Statistical analyses were performed using a GraphPad Prism software package (GraphPad Software, San
Diego, CA). The one-way ANOVA test was used, and
p < 0.05 was considered as statistically significant.
Results
Optical density determination of HSA
glycation is highest for extensively glycated
samples
Figure 1 (a) shows the absorbance of HSA incubated with or without glucose in PBS, for 5 weeks or 60
days. HSA incubated with glucose for 60 days showed
the highest values of absorbance units in the studied
wavelength when compared to all other samples. We
noticed as well that HSA incubated for 60 days without
glucose showed higher values of absorbance units
than HSA incubated for 5 weeks under the same conditions.
Figure 1 (b) shows the absorbance of HSA incubated
with or without glucose in a sodium phosphate buffer,
for 5 weeks or 60 days. Again, HSA incubated with glucose for 60 days showed the highest values of absorbance units in the studied wavelength when compared
to all other samples.
Long-term incubation of human monocyte-derived macrophages with extensively
glycated HSA upregulates release of VEGF
When human monocyte-derived macrophages were
stimulated with 600 mg/ml extensively glycated HSA
(9 weeks with 1.67 M glucose) in NaH2PO4, VEGF release was significantly increased (p < 0.01 by one-way
ANOVA versus unstimulated cells, or versus cells incubated with HSA alone; figure 2). There was no comparable induction of VEGF by minimally glycated HSA
(5 weeks with 50 mM glucose) in this buffer, or with
samples minimally and extensively glycated in PBS.
CML-modified BSA is an inducer of VEGF
production in cultured human monocyte-derived macrophages
To determine the effect of CML-modified BSA, prepared by incubating BSA with sodium cyanoborohydride and glyoxylic acid in a NaH2PO4 buffer for 24
hours, human monocyte-derived macrophages were
incubated for 4–24 hours in the presence of 1–9.5 mg/ml
CML-modified BSA or unmodified BSA. Significant
VEGF production was only seen with 9.5 mg/ml CML-modified BSA (184 ± 8 pg/ml versus 75 ± 15 pg/ml
in the presence of BSA alone; p < 0. 001; figure 3),
and was undetectable after incubation times of less
than 24 hours.
Discussion
Diabetes is a widespread disease with multiple complications that affect both the microvasculature and macrovasculature. Considerable evidence now supports
a major role for AGE in the development of diabetes and
diabetes related pathological conditions, such as retinopathy [17–19].
The formation and accumulation of AGE has been
known to progress at an accelerated rate in diabetes.
Recent understanding of this process has confirmed that
AGE are implicated in the pathogenesis of diabetic va-
483
A
B
Figure 1. Extensively glycated HSA show the highest values of absorbance units. A. HSA highly modified by AGE was prepared by incubation of HSA (50 mg/ml) with 1.67 M glucose in 150 mM sodium phosphate buffer pH 7.4 at 37°C for 60 days. HSA without glucose
was incubated in the same buffer for 60 days as a control. HSA minimally modified by glucose derived AGE was prepared by incubation
of HSA (50 mg/ml) in a 150 mM sodium phosphate buffer of pH 7.4 at 37°C for 5 weeks. HSA without glucose was incubated in the
same buffer for 5 weeks as a control. B. HSA highly modified by AGE was prepared by incubation of HSA (50 mg/ml) with 1.67 M glucose in PBS, pH 7.4 at 37°C for 60 days. HSA without glucose was incubated in the same buffer for 60 days as a control. HSA minimally
modified by glucose derived AGE was prepared by incubation of HSA (50 mg/ml) in PBS, pH 7.4 at 37°C for 5 weeks. HSA without glucose was incubated in the same buffer for 5 weeks as a control
Rycina 1. Ekstensywnie glikowane HSA wykazuje najwyższe wartości absorbancji. A. HSA w znacznym stopniu zmodyfikowane przez
AGE przygotowano, inkubując HSA (50 mg/ml) z 1,67 M roztworem glukozy w 150 mM buforze sodowo-fosforanowym (pH 7,4) w temperaturze 37°C przez 60 dni. W tym samym buforze inkubowano przez 60 dni HSA bez glukozy jako roztwór kontrolny. HSA w niewielkim
stopniu zmodyfikowane przez AGE przygotowano, inkubując HSA (50 mg/ml) w 150 mM buforze sodowo-fosforanowym (pH 7,4) w temperaturze 37°C przez 5 tygodni. W tym samym buforze inkubowano przez 5 tygodni HSA bez glukozy jako roztwór kontrolny. B. HSA
w znacznym stopniu zmodyfikowane przez AGE przygotowano, inkubując HSA (50 mg/ml) z 1,67 M roztworem glukozy w PBS (pH 7,4)
w temperaturze 37°C przez 60 dni. W tym samym buforze inkubowano przez 60 dni HSA bez glukozy jako roztwór kontrolny. HSA w niewielkim stopniu zmodyfikowane przez AGE przygotowano, inkubując HSA (50 mg/ml) w PBS (pH 7,4) w temperaturze 37°C przez 5 tygodni. W tym samym buforze inkubowano przez 5 tygodni HSA bez glukozy jako roztwór kontrolny
scular complications [20, 21]. One of the potential pathogenic mechanisms linking AGE to diabetes related
vascular complications is VEGF [9, 22, 23]. Macrophages play a role in the progression of any vascular injury
[26], which develops during the progression of diabetes. These cells take up AGE through AGE-specific cell
surface receptors [25]. AGE are known as well to exhibit
a growth inhibitory action on pericytes, which would
lead to pericyte loss, the earliest histological hallmark in
diabetic retinopathy [20].
In view of these literature data, we decided to look at
different methods of albumin glycation and its effect on
VEGF production. We used HSA, either extensively glycated (9 weeks with 1.67 M glucose), or minimally glycated (5 weeks with 50 mM glucose), in either PBS or
a sodium phosphate buffer. Absorbance and mass spectrometry analyses suggested that HSA extensively glycated in a sodium phosphate buffer showed the greatest degree of lysine modification by glucose. Elutriated monocytes were differentiated to macrophages in
the presence of M-CSF [13]. When these human mono-
484
cyte-derived macrophages were stimulated with HSA
extensively glycated in a sodium phosphate buffer, we
observed a significantly increased VEGF release compared to unstimulated cells, or cells incubated with HSA.
There was no comparable induction of VEGF by HSA
minimally glycated in this buffer, or with samples minimally and extensively glycated in PBS. Finally, we chose
to prepare CML adducts, since CML-modified proteins
are the predominant AGE in vivo, and play a central role
in disease pathogenesis. In particular, CML provide an
important link between AGE and chronic inflammation
without loss of glycaemic control, since these products
are likely to form in diseases associated with oxidative
stress, such as rheumatoid arthritis. Addition of CML-BSA, prepared by incubation in the presence of sodium
cyanoborohydride and glyoxylic acid, strikingly upregulated the release of VEGF.
The identity of the receptor on macrophages involved in the induction of VEGF release is at present
unclear. Cell surface AGE receptors (including AGE-R1, -R2 and -R3) have been identified on macropha-
Figure 2. Induction of VEGF release from human macrophages by HSA extensively glycated in NaH2PO4. Human monocyte-derived macrophages were incubated for 24 hours in the presence of 600 mg/ml HSA, minimally modified by 50 mM glucose for 5 weeks or extensively modified by 1.67 M glucose for 9 weeks, in either PBS or a 150 mM NaH2PO4 buffer. HSA without glucose was incubated in the
same buffers as a control. LPS (10 ng/ml) was used as a control stimulus. Data shown are VEGF release (mean pg/ml ± SEM), and are
from a total of 3 experiments
Rycina 2. Indukcja wydzielania VEGF przez ludzkie makrofagi po zastosowaniu HSA ekstensywnie glikowanego w NaH2PO4. Makrofagi
ludzkie indukowano przez 24 godziny w obecności 600 mg/ml HSA nieznacznie zmodyfikowanego przez 50 mM roztwór glukozy przez
5 tygodni lub znacznie zmodyfikowanego przez 1,67 M roztwór glukozy przez 9 tygodni, w PBS lub buforze sodowo-fosforanowym.
W tych samych buforach inkubowano HSA bez glukozy jako roztwór kontrolny. Jako bodziec kontrolny użyto LPS.
Przedstawiono uwalnianie VEGF (średnia [pg/ml] ± SEM); dane pochodzą z trzech eksperymentów
ges, monocytes and endothelial cells [28], but receptors include scavenger receptor class A (ScR-A), lectin-like oxidised low density lipoprotein receptor-1
(LOX-1) and RAGE, a multi-ligand member of the immunoglobulin superfamily of cell surface molecules,
expressed in multiple tissues and interacting also with
other ligands [27]. The signalling pathways activated
by AGE to induce responses such as VEGF, cytokines
and tissue factor probably involve mitogen-activated
protein kinases and NFkB. For example, endothelial
cells upregulate tissue factor and VCAM-1 in response
to AGE through NFkB [14, 28]. AGE-induced VEGF
expression has been shown to occur via NFkB [29],
and we have shown that VEGF expression in macrophages is NFkB-dependent [14]. The activation of the
NFkB pathway in macrophages stimulated with HSA
modified by glucose-derived AGE and CML-BSA is currently being investigated in our laboratory. In a study
published by Festa et al, the authors examined the
expression of AGE binding sites on peripheral mono-
cytes, serum levels of AGE and AGE-induced cytokine
production in patients with insulin-dependent diabetes
mellitus, compared to healthy control subjects. They
found that AGE-binding capacity was significantly increased in patients, and that there was only one class
of binding sites. They also found much higher levels of
circulating AGE in patients as compared to controls.
The increased presence of AGE-binding proteins on
diabetic monocytes did not result in enhanced cytokine production after activation by AGE [30].
In summary, the interactions between blood borne
AGE, cytokines, growth factors, and the different vessel
wall cell types which contribute to atherogenesis and
other vascular complications, are extremely complex
and multi-factorial. Our results show that VEGF production in human monocyte/macrophages is augmented in
the presence of proteins highly modified by AGE. Thus,
AGE-induced activation of macrophages may contribute to vascular complications by regulation of angiogenic
processes.
485
Figure 3. CML-modified BSA upregulates VEGF production by human monocyte-derived macrophages BSA. Human monocyte-derived
macrophages were incubated in the absence or presence of CML-modified BSA, prepared by incubating BSA with sodium cyanoborohydride and glyoxylic acid in 0.2 M NaH2PO4 buffer for 24 hours. VEGF production by human monocyte-derived/macrophages incubated for
24 hours in the presence of 1–9.5 mg/ml CML-modified BSA or unmodified BSA
Rycina 3. Podwyższanie produkcji VEGF w ludzkich makrofagach przez modyfikowaną CML. Ludzkie makrofagi inkubowano z lub bez
BSA modyfikowanego CML (przygotowanego przez inkubację BSA z cyjanoborowodorkiem sodu i kwasem glioksylowym w 0,2 M buforze sodowo-fosforanowym przez 24 godziny). Wytwarzanie VEGF przez makrofagi ludzkie inkubowane przez 24 godziny w obecności modyfikowanego BSA w stężeniach 1–9,5 mg/ml lub niemodyfikowanego BSA
Acknowledgements
The Kennedy Institute of Rheumatology is a division
of Imperial College, London, and receives a Core Grant
from arc (Registered Charity No. 207711). Dr Magdalena
Pertyńska-Marczewska was supported by a NATO
Science Fellowships Programme. The expert advice of
Dr David Moyes, Dr Claudia Monaco and Professor Brian
Foxwell is gratefully acknowledged.
Abstract
Background. It is becoming apparent that diabetes results in
the increased expression of angiogenic growth factors in numerous tissues. Angiogenesis is regulated by growth factors,
particularly the vascular endothelial growth family (VEGF) of
proteins. During the course of diabetes, glucose binds to protein amino residues and forms early glycation products. The
final Maillard reaction leads to the production of advanced
glycation end products (AGE), and is slow, irreversible and
dependent on plasma glucose concentrations. AGE are now
486
thought to contribute to the development of chronic vascular
dysfunction, including the complications of diabetes.
Aim. To determine VEGF production in human monocyte-derived macrophages stimulated with glycated albumin, or
Ne-(carboxymethyl)lysine (CML)-modified albumin.
Methods. Human serum albumin (HSA), modified by glucose-derived AGE, was prepared by incubation with glucose
for differing periods of time. Alternatively, bovine serum albumin (BSA) was incubated with sodium cyanoborohydride and
glyoxylic acid in a NaH2PO4 buffer for 24 hours, to produce
Ne-(carboxymethyl)lysine-modified BSA (CML-BSA).
Results. Human monocyte-derived macrophages stimulated
with 600 mg/ml HSA extensively glycated (9 weeks with 1.67 M
glucose) in NaH2PO4, showed significant VEGF release. Human monocyte-derived macrophages were also incubated for
4–24 hours in the presence of 1–9.5 mg/ml CML-modified BSA
or unmodified BSA. However, significant VEGF production was
only seen with 9.5 mg/ml CML-modified BSA and was undetectable at incubation times of less than 24 hours.
Conclusions. In summary, albumin extensively modified by
glucose-derived AGE and by CML induced the release of
VEGF, suggesting that AGE-induced activation of macrophages may contribute to vascular complications by the
regulation of angiogenesis.
key words: vascular endothelial growth factor (VEGF),
human monocyte-derived macrophages, diabetic vascular
complications
References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
Ahmed M.U., Thorpe S.R., Baynes J.W. Identification of N
epsilon-carboxymethyllysine as a degradation product of
fructoselysine in glycated protein. J. Biol. Chem. 1986; 261:
4889–4894.
Chappey O., Dosquet C., Wautier M..P., Wautier J.L. Advanced glycation end products, oxidant stress and vascular
lesions. Eur. J. Clin. Invest. 1997; 27: 97–108.
Krolewski A.S., Warram J.H., Valsania P., Martin B.C., Laffel L.M.,
Christlieb A.R. Evolving natural history of coronary artery disease in diabetes mellitus. Am. J. Med. 1991; 90:
S56–S61.
Schmidt A.M., Hori O., Chen J.X., Li J.F., Crandall J., Zhang J.,
Cao R., Yan S.D., Brett J., Stern D. Advanced glycation endproducts interacting with their endothelial receptor induce
expression of vascular cell adhesion molecule-1 (VCAM-1)
in cultured human endothelial cells and in mice. A potential
mechanism for the accelerated vasculopathy of diabetes. J.
Clin. Invest. 1995; 96: 1395–1403.
Basta G., Lazzerini G., Massaro M., Simoncini T., Tanganelli P.,
Fu C., Kislinger T., Stern D.M., Schmidt A.M., De Caterina R.
Advanced glycation end products activate endothelium
through signal-transduction receptor RAGE: a mechanism
for amplification of inflammatory responses. Circulation 2002;
105: 816–822.
Nishikawa T., Edelstein D., Yamagishi X. L. et al. Normalizing mitochondrial superoxide production blocks three
pathways of hyperglycaemic damage. Nature 2000; 404:
787–790.
Wautier J. L., Wautier M. P., Schmidt A. M. et al. Advanced
glycation end products (AGE) on the surface of diabetic erythrocytes bind to the vessel wall via a specific receptor inducing oxidant stress in the vasculature: a link between surface-associated AGE and diabetic complications. Proc. Natl.
Acad. Sci. USA 1994; 91: 7742–7746.
Ido Y., Chang K.C., Lejeune W.C. et al. Vascular dysfunction
induced by AGE is mediated by VEGF via mechanisms involving reactive oxygen species, guanylate cyclase, and protein kinase C. Microcirculation 2001; 8: 251–263.
Lu M., Kuroki M., Amano S. Advanced glycation end products increase retinal vascular endothelial growth factor expression. J. Clin. Invest. 1998; 101: 1219–1224.
Treins C., Giorgetti-Peraldi S., Murdaca J., van Obberghen E.
Regulation of vascular endothelial growth factor expression
by advanced glycation end products. J. Biol. Chem. 2001;
276: 43836–43841.
Urata Y., Yamaguchi M., Higashiyama Y. Reactive oxygen
species accelerate production of vascular endothelial
growth factor by advanced glycation end products in
RAW264. 7 mouse macrophAGE. Free Radic. Biol. Med.
2002; 32: 688–701.
Krolewski A.S. , Warram J.H., Valsania P., Martin B.C., Laffel L.M.,
Christlieb A.R. Evolving natural history of coronary artery disease in diabetes mellitus. Am. J. Med. 1991; 90: S56–S61.
Westwood M.E., Argirov O.K., Abordo E.A., Thornalley P.J.
Methylglyoxal — modified arginine residues — a signal for
receptor — mediated endocytosis and degradation of proteins by monocytic THP-1 cells. Biochim. Biophys. Acta 1997;
1356: 84–94.
Kislinger T., Fu C., Huber B. N(epsilon)-(carboxymethyl)lysine
adducts of proteins are ligands for receptor for advanced
glycation end products that activate cell signaling pathways
and modulate gene expression. J. Biol. Chem. 1999; 274:
31740–31749.
15. Foxwell B., Browne K., Bondeson J. Efficient adenoviral infection with IkappaB alpha reveals that macrophage tumor
necrosis factor alpha production in rheumatoid arthritis is NF-kappaB dependent. Proc. Natl. Acad. Sci. USA 1998; 95:
8211–8215.
16. Kiriakidis S., Andreakos E., Monaco C., Foxwell B., Feldmann M.,
Paleolog E. et al. VEGF expression in human macrophages
is NF-κB-dependent: studies using adenoviruses expressing the endogenous NF-κB inhibitor IkBa and a kinase defective form of the IkB kinase 2. Journal of Cell Science 2003;
116: 665–674.
17. Hammes H.P., Alt A., Niwa T. et al. Differential accumulation
of advanced glycation end products in the course of diabetic
retinopathy. Diabetologia 1999; 42: 728–736.
18. Stitt A.W., Moore J.E., Sharkey J.A. et al. Advanced glycation
end products in vitreous: Structural and functional implications for diabetic vitreopathy. Invest. Ophthalmol. Vis. Sci.
1998; 39: 2517–2523.
19. Stitt A.W. Advanced glycation: an important pathological event
in diabetic and age related ocular disease. Br. J. Ophthalmol. 2001; 85: 746–753.
20. Endo M., Yanagisawa K., Tsuchida K. et al. Increased levels
of vascular endothelial growth factor and advanced glycation end products in aqueous humor of patients with diabetic
retinopathy. Horm. Metab. Res. 2001; 33: 317–322.
21. Chiarelli F., de Martino M., Mezzetti A. et al. Advanced glycation end products in children and adolescents with diabetes:
relation to glycemic control and early microvascular complications. J. Pediatr. 1999; 134: 486–491.
22. Hirata C., Nakano K., Nakamura N. et al. Advanced glycation end products induce expression of vascular endothelial
growth factor by retinal Muller cells. Biochem. Biophys. Res.
Commun. 1997; 236: 712–715.
23. Murata C., Nagai R., Ishibashi T., Inomuta H., Ikeda K., Horiuchi S. The relationship between accumulation of advanced
glycation end products and expression of vascular endothelial growth factor in human diabetic retinas. Diabetologia 1997;
40: 764–769.
24. Radoff S., Cerami A., Vlassara H. Isolation of surface binding protein specific for advanced glycosylation end products
from mouse macrophage-derived cell line RAW 264. 7. Diabetes 1990; 39: 1510–1518.
25. Schmidt A.M., Yan S.D., Yan S.F., Stern D.M. The multiligand
receptor RAGE as a progression factor amplifying immune and
inflammatory responses. J. Clin. Invest. 2001; 108: 949–955.
26. Stitt A.W., He C., Vlassara H. Characterization of the advanced
glycation end-product receptor complex in human vascular
endothelial cells. Biochem. Biophys. Res. Commun. 1999;
256: 549–556.
27. Schmidt A.M., Yan S.D., Yan S.F., Stern D.M. The multiligand
receptor RAGE as a progression factor amplifying immune and
inflammatory responses. J. Clin. Invest. 2001; 108: 949–955.
28. Bierhaus A., Illmer T., Kasper M. et al. Advanced glycation
end product (AGE)-mediated induction of tissue factor in
cultured endothelial cells is dependent on RAGE. Circulation
1997; 96: 2262–2271.
29. Lu M., Kuroki M., Amano S. et al. Advanced glycation end
products increase retinal vascular endothelial growth factor
expression. J. Clin. Invest. 1998; 101: 1219–1224.
30. Festa A., Schmolzer B, Schernthaner G., Menzel E. Differential expression of receptors for advanced glycation end products on monocytes in patients with IDDM. Diabetologia 1998;
41: 674–680.
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