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Curcumin inhibits VEGF-mediated angiogenesis inhuman intestinal microvascular endothelial cellsthrough COX-2 and MAPK inhibition
D G Binion,
1
M F Otterson,
2
P Rafiee
2
1
Department of Medicine,Medical College of Wisconsin,Milwaukee, Wisconsin, USA;
2
Department of Surgery,Medical College of Wisconsin,Milwaukee, Wisconsin, USACorrespondence to:Dr P Rafiee, Department ofSurgery, Medical College ofWisconsin, 8701 WatertownPlank Road, Milwaukee, WI53226, USA; prafiee@mcw.eduRevised 16 May 2008Accepted 10 June 2008PublishedOnlineFirst2July 2008This paper is freely availableonline under the BMJ Journalsunlocked scheme, see http:// gut.bmj.com/info/unlocked.dtl
ABSTRACTBackground:
Angiogenesis, the growth of new bloodvessels, is a critical homeostatic mechanism whichregulates vascular populations in response to physiologi-cal requirements and pathophysiological demand, includ-ing chronic inflammation and cancer. The importance ofangiogenesis in gastrointestinal chronic inflammation andcancer has been defined, as antiangiogenic therapy hasdemonstrated benefit in models of inflammatory boweldisease and colon cancer treatment. Curcumin is a naturalproduct undergoing evaluation for the treatment ofchronic inflammation, including inflammatory boweldisease (IBD). The effect of curcumin on human intestinalangiogenesis is not defined.
Methods:
The antiangiogenic effect of curcumin on invitro angiogenesis was examined using primary culturesof human intestinal microvascular endothelial cells(HIMECs), stimulated with vascular endothelial growthfactor (VEGF).
Results:
Curcumin inhibited proliferation, cell migrationand tube formation in HIMECs induced by VEGF.Activation of HIMECs by VEGF resulted in enhancedexpression of cyclo-oxygenase-2 (COX-2) mRNA, proteinand prostaglandin E
2
(PGE
2
) production. Pretreatment ofHIMECs with 10
m
M curcumin as well as 1
m
M NS398, aselective inhibitor of COX-2, resulted in inhibition of COX-2at the mRNA and protein level and PGE
2
production.Similarly COX-2 expression in HIMECs was significantlyinhibited by Jun N-terminal kinase (JNK; SP600125) andp38 mitogen-activated protein kinase (MAPK; SB203580)inhibitors and was reduced by p44/42 MAPK inhibitor(PD098059).
Conclusions:
Taken together, these data demonstrate animportant role for COX-2 in the regulation of angiogenesisin HIMECs via MAPKs. Moreover, curcumin inhibitsmicrovascular endothelial cell angiogenesis throughinhibition of COX-2 expression and PGE
2
production,suggesting that this natural product possesses anti-angiogenic properties, which warrants further investiga-tion as adjuvant treatment of IBD and cancer.
 Vascular endothelial growth factor (VEGF) playsan essential role in endothelial proliferation andangiogenesis during embryonic development aswell as periods of increased physiological, demandincluding the menstrual cycle, pregnancy andwound healing.
1 2
Enhanced expression of VEGFalso occurs in disease conditions leading topathological angiogenesis including chronic inflam-mation (ie, rheumatoid arthritis, psoriasis, inflam-matory bowel disease (IBD)), diabetic retinopathy and adenocarcinoma.
3
The importance of angio-genesis in disease processes has been demonstratedby the success of antiangiogenic therapeutic trials,which are approved for the treatment of advancedcolorectal adenocarcinoma.
4
 VEGF plays a key rolein cancer biology and contributes to tumourneovascularisation in response to the increaseddemand for delivery of nutrients and oxygen.
5–7
Inthe setting of chronic inflammation, antiangio-genic therapy has shown beneficial effects inanimal models of IBD (Crohn’s disease, ulcerativecolitis)
8
as well as open-label trials of the com-pound thalidomide in refractory Crohn’s disease.Thecyclo-oxygenase(COX)enzymesareinvolvedin numerous physiological responses includinginflammation, where they catalyse the synthesis of prostaglandins (PGs) from arachidonic acid. COX-1is one of the two COX isoforms, and is responsiblefor maintaining normal physiological functions; it isexpressed constitutively in most tissues. In contrast,COX-2 is an early response gene induced by growthfactors, proinflammatory cytokines, tumour promo-ters and bacterial toxins.
9–11
Inhibition of COX-2 by non-steroidal anti-inflammatory drugs (NSAIDs)results in inhibition of angiogenesis and down-regulation of angiogenic factors such as VEGF andbFGF-2 (basic fibroblast growth factor).
12–14
Inhuman colorectal adenocarcinoma and other malig-nancies such as breast, cervical, prostate and lungtumours, increased COX-2 expression has beenreported.
15 16 
In mice, inhibition of COX-2 has beenshown to protect against intestinal polyposis.
17
Theprecise mechanisms whereby COX-2 contributes totumourigenesis include effects on the epithelium,but additional effects on non-epithelial populationsincluding the microvascular endothelium have alsobeen suggested.
11
Curcumin, the major yellow colouring pigmentfound in the household spice turmeric (
Curcumalonga
Linn, Zingiberaceae), has been used forcenturies in food preparation as well as in Ayurvedic traditional medicine to treat inflamma-tory disorders.
18
Curcumin has low toxicity and hasbeen shown to benefit the treatment of chronic gutinflammation in animal models, as well as showingbenefit in a randomised cross-over trial in thetreatment of ulcerative colitis.
19
 Also, curcumin hasbeen shown to have antineoplastic potential,inhibiting the development of chemically inducedtumours of the oral cavity, skin, forestomach,duodenum and colon in rodents.
20–23
The effect of curcumin on pathological angiogenesis associatedwith gastrointestinal disease processes has notbeen defined.Our laboratory has focused investigation on themicrovascular endothelial biology of the human
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gastrointestinal tract, utilising primary cultures of humanintestinal microvascular endothelial cells (HIMECs).Previously, we have shown that VEGF leads to proliferation of HIMECs,
24
triggering dephosphorylation, translocation andactivation of NFAT (nuclear factor of activated T cells) inHIMECs.
25
 VEGF activates various signalling pathways such asphosphatidylinositol 3-kinase (PI3K)/Akt, protein kinase C(PKC) and mitogen-activated protein kinase (MAPK) cascades.
26 
However, the signalling pathways by which VEGF regulatesCOX expression in HIMECs are not fully characterised.In the present study, we examined the effect of curcumin andMAPK inhibitors on COX-2 gene expression and angiogenesis inHIMECs following VEGF stimulation. We have shown thatCOX-2 plays an important role in VEGF-induced angiogenesisvia MAPKs, and curcumin blocks both COX-2 expression andangiogenesis induced by VEGF. These results may provide amechanistic understanding for the beneficial effects of curcuminin conditions including chronic inflammation and cancer, wherepathological neovascularisation is associated with an enhancedexpression of VEGF.
MATERIALS AND METHODSReagents
Endothelial cell growth supplement (ECGS) was from UpstateCell Signaling Solutions (Temecula, California, USA). RPMI1640 medium, fetal bovine serum (FBS), MCDB-131 mediumand PSF (penicillin/streptomycin/fungizone) were obtainedfrom Invitrogen (Carlsbad, California, USA). Human plasmafibronectin was purchased from Chemicon International(Temecula, California, USA). Porcine heparin was from SigmaChemical Co. (St Louis, Missouri, USA). The recombinanthuman VEGF, antibodies to intercellular adhesion molecule 1(ICAM-1), vascular cell adhesion molecule (VCAM) and E-selectin were purchased from R&D Systems (Minneapolis,Minnesota, USA). The COX-1/-2 antibodies were obtainedfrom Santa Cruz Biotechnology (Santa Cruz, California, USA).The selective COX-2 inhibitor NS398 and carbacyclin (stableanalogue of PGI
2
) were obtained from Cayman Chemical (Ann Arbor, Michigan, USA). Antibodies against phosphorylated andnon-phosphorylated MAPK family members (p44/42 MAPK,p38 MAPK and JNK (Jun N-terminal kinase)) were from CellSignaling Technology (Danvers, Massachusetts, USA). TheMAPK inhibitors (PD098059, SB203580 and SP600125) wereobtained from Calbiochem (La Jolla, California, USA). Immun-Star and all other electrophoresis reagents were from Bio-Rad(Hercules, California, USA). Oligonucleotides and primers werepurchased from IDT (Integrated DNA Technologies, Coralville,Iowa, USA). Fluorescein-conjugated phalloidin was fromMolecular Probes (Eugene, Oregon, USA). Unless otherwiseindicated, all other chemicals used in this study were purchasedfrom Sigma-Aldrich. All experiments were approved by theInstitutional Review Board of the Medical College of Wisconsin.
HIMEC isolation and culture
HIMECs were isolated and cultured as previously described.
24
Experiments were performed on three independent HIMEC linesunless otherwise specified. All images displayed were a represen-tative result of one of the three independent experiments.
Activation and pharmacological modulation of HIMECs
HIMEC activation was achieved following VEGF (50 ng/ml)stimulation for specified time periods. Curcumin (10
m
M),NS398 (1
m
M), SB203580 (5
m
M), PD098059 (10
m
M) andSP600125 (10
m
M) were used to determine the effect of theseinhibitors on COX-2 expression and angiogenesis.
Cell proliferation assay 
 A total of 3
6
10
4
HIMECs per well were seeded onto fibronectin-coated 24-well plates, and proliferation assays were performedas previously described.
25
 After pretreatment with 10
m
Mcurcumin and 1
m
M NS398, 5
m
M SB203580, 10
m
MPD098059 and 10
m
M SP600125 for 30 min at 37
u
C, cells werestimulated with VEGF (50 ng/ml) for 12, 24, 48 and 72 h, or leftuntreated. Then, cells were re-suspended and counted in aCoulter Counter (Coulter, Brea, California, USA). In parallelexperiments, cell viability was assessed by trypan blue exclusionand was
.
95%. Each condition was assessed in triplicate.CellularDNAsynthesiswasassessedby[
3
H]thymidineuptake.
25
HIMECs were pulsed with [
3
H]thymidine (1
m
Ci/ml; Amersham, Arlington Heights, Illinois, USA) and washed with 5% (v/v)trichloroacetic acid (2
6
) prior to fixation. Using 0.5 N NaOH, theDNAwas precipitated, and supernatants were quantified in a betacounter. Each condition was assessed in triplicate.
Microscopic wounding assay 
To assess the effect of curcumin on HIMEC growth followingangiogenic stimuli, a microscopic wounding assay was per-formed as described earlier.
25
In brief, a HIMEC confluentmonolayer was scraped along a straight line, and the remainingmonolayer was then incubated with growth medium (withoutECGS), and cells were pretreated for 30 min at 37
u
C with orwithout curcumin (10
m
M) or NS398 (1
m
M). Then, cells werestimulated by addition of VEGF (50 ng/ml) or left untreated.The migration of HIMECs across the demarcation line wasmonitored using an inverted microscope. At each time point (0,24, 48 and 72 h), 10 random fields were counted in a blindedfashion using an ocular grid. Data were expressed as cells/mm
2
,and each condition was assessed in triplicate.
Endothelial cell chemotaxis assay 
HIMECs (3
6
10
4
cells/cm
2
) were cultured on fibronectin-coatedpolycarbonate filters (8
m
m pore size, BD Biosciences, Bedford,Massachusetts, USA) as previously described.
25
 After incubationin overnight medium containing 2% FBS, HIMECs wereincubated with curcumin (0–20
m
M) or NS398 (0–10
m
M) for 2h, and buffers containing VEGF (50 ng/ml) were poured into thelower compartment of the 12-well plates. When indicated, PGE
2
(0.1–1
m
M) was added to both upper and lower chambers. Afterovernight incubation, cell culture inserts were removed and theupper surface of the membrane was gently wiped to remove non-migrated cells. Filters were stained with DiffQuik (BaxterScientific, McGraw, Illinois, USA), air-dried, and mounted ontoglass slides. Migrated HIMECs adherent to the lower side of themembrane were counted (10 random high-power fields (40
6
) percondition in a blinded fashion). Cell viability was
.
95% asassessed by trypan blue exclusion. Each condition was assessed intriplicate, and data were expressed as a mean (SD).
Matrigel in vitro tube formation assay 
HIMEC tube formation was assessed using Matrigel, asdescribed previously.
25
 Where indicated, the culture mediumwas supplemented with various inhibitors as above, whilecontrol wells contained no inhibitors. Using an inverted phasecontrast microscope, HIMEC tube formation was assessed. Fivehigh-power fields per condition were examined and experimentswere repeated in three independent HIMEC cultures.
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ELISAs of PGE
2
and 6-keto PGF
1
a
in HIMEC culture medium
Confluent HIMEC monolayers were assayed as previously described.
27
Briefly, HIMECs were pretreated for 2 h withcurcumin (0–20
m
M) then stimulated with 50 ng/ml VEGF for 8h. The concentration of PGE
2
and 6-keto PGF
1
a
(the stablemetabolite of PGI
2
) in the culture supernatant was determinedusing a commercial ELISA (Cayman Chemical). To determineCOX isozymes which produce PGE
2
and PGI
2
, HIMECs werepretreated with NS398 (0–10
m
M), the COX-2-specific inhibi-tor, for 2 h then stimulated with 50 ng/ml VEGF for 8 h. Theconcentration of PGE
2
and 6-keto PGF
1
a
was determined asdescribed above. Experiments were carried out in triplicate, andresults are shown as mean pg/ml (SD).
RNA preparation and semi-quantitative reverse transcription–PCR (RT–PCR)
COX-1 and COX-2 mRNA expression were determined asdescribed previously.
25
PCR amplifications were performed asfollows: 30 cycles for COX-1 (94
u
C for 1 min, 56 
u
C for 1 min,72
u
C for 1 min), 35 cycles for COX-2 (94
u
C for 1 min, 54
u
C for1 min, 72
u
C for 1 min) and 25 cycles for
b
-actin (94
u
C for1 min, 60
u
C for 1 min, 72
u
C for 1 min), using COX-1 forward(5
9
-TGC CCA GCT CCT GGC CCG CCG CT-3
9
) and reverse(5
9
-TTC AAA TGA GAT TGT GGG AAA ATT GTC-3
9
); COX-2 forward (5
9
- TCA AAT GAG ATT GTG GGA AAA TTG-3
9
)and reverse (5
9
-TCT AGT AGA GAC GGA CTC ATA GAA-3
9
);and
b
-actin forward (5
9
-CCA GAG CAA GAG AGG CAT CC-3
9
)and reverse (5
9
-CTG TGG TGG TGA AGC TGT AG-3
9
) specificprimers, followed by final extension for 7 min at 72
u
C. The PCR products were visualised on 1.2% agarose gels stained withethidium bromide. RNA solution without reverse transcriptionwas used as negative control (no RT), and
b
-actin served as aninternal control.
Western blot analysis
Confluent HIMEC monolayers in 35 mm culture dishes (one dishper condition) were pretreated with various inhibitors for 30 minor left untreated before VEGF activation (50 ng/ml) for differenttime periods. Sodium dodecylsulfate–polyacrylamide gel electro-phoresis (SDS–PAGE) and western blot analysis were performedusing antibodies to COX-1, COX-2 and MAPKs as describedpreviously.
25
Detection was by secondary antibody coupled tohorseradish peroxidase (HRP) and Immun-Star (Bio-Rad).
Immunofluorescence staining
HIMEC monolayers were grown on coverslips to 80% confluence.Following curcumin or NS398 treatment and VEGF activation,monolayers were rinsed once in phosphate-buffered saline (PBS),fixed with cold methanol for 30 min and blocked with 5% bovineserum albumin in PBS with Ca
2
+
and Mg
2
+
for 60 min. UsingCOX-2 antibody, followed by a fluorescein isothiocyanate(FITC)-conjugated secondary antibody (Santa CruzBiotechnology), the effect of curcumin on COX-2 expressionwas visualised. Coverslips were mounted on Superfrost slides(Fisher Scientfic) with Prolong Antifade mounting medium(Invitrogen) and visualised using a fluorescence microscope(Olympus BX-40) and a Leica DFC 300FX camera.
Assessment of cell adhesion molecule (CAM) surface expressionby tumour necrosis factor
a
(TNF
a
)/lipopolysaccharide (LPS) inHIMECs
CAM surface expression in HIMECs was assessed followingTNF
a
 /LPS (100 U/ml TNF
a
, 1
m
g/ml LPS) activation with orwithout 10
m
M curcumin pretreatment using radioactiveimmunoassay (RIA) and flow cytometry (fluorescence activatedcell sorting (FACS)) as described previously.
28 29
Leucocyte adhesion assay on HIMECs
Leucocyte–HIMEC interaction with or without 10
m
M curcu-min pretreatment was assessed using a low shear stress flowadhesion assay and U-937 cells as described previously.
28 29
RESULTSVEGF induced increased COX-2 expression in HIMECs
 Activation of HIMECs with 50 ng/ml VEGF resulted inenhanced COX-2 expression at the mRNA level as detected by RT–PCR using COX-2 primers. Enhanced COX-2 mRNexpression was time dependent, increasing by 3 h, and decliningby 18 h (fig 1A).
b
-Actin gene expression was used as an internalcontrol in these experiments. In marked contrast, levels of COX-1 mRNA expression remained unchanged following VEGFstimulation of HIMECs (Fig. 1A).Next we determined the effect of VEGF on COX-2 proteinexpression by western blotting using a specific COX-2 antibody. VEGF strongly and time dependently (6–24 h) enhanced theexpression of COX-2 protein in HIMECs (fig 1B). There was nodetectable change in the level of COX-1 protein after VEGFstimulation (fig 1B).Corresponding to the effect of VEGF on COX-2 mRNA andprotein expression, the ELISA results from the HIMEC culturesupernatant demonstrated that VEGF (50 ng/ml) stimulationfor 12 h significantly increased PGE
2
and 6-keto PGF
1
a
produc-tion (fig 1C).
Curcumin inhibits COX-2 expression and PGE
2
production inHIMECs
Next we examined the effect of curcumin on COX-2 gene andprotein expression. Pretreatment of HIMECs with curcuminabolished VEGF induction of COX-2 mRNA expression in adose-dependent fashion (fig 2A). Consistent with the geneexpression data, curcumin pretreatment of HIMECs inhibitedCOX-2 protein expression at 1
m
M, with increasing effect at10
m
M curcumin, while 20
m
M curcumin completely abolishedCOX-2 expression following VEGF activation (fig 2B). Theselective inhibitor of COX-2, NS398 (1
m
M), abolished COX-2mRNA and protein expression in HIMECs following VEGFactivation (not shown). In addition, immunofluorescencestaining of HIMECs pretreated with either 10
m
M curcuminor 1
m
M NS398 demonstrated inhibition of COX-2 expressionfollowing VEGF activation (fig 2C).Corresponding with the effect on COX-2 expression, curcu-min inhibited both PGE
2
and 6-keto PGF
1
a
production in a dose-dependent fashion as determined by ELISA measurement of HIMEC culture media (fig 2D). PGE
2
and 6-keto PGF
1
a
production were completely inhibited by 1
m
M NS398 (pre-treatment), indicating that production of this prostanoid isdependent on COX-2 activity in HIMECs (fig 2E).
Curcumin inhibits HIMEC growth, proliferation, migration andtube formation
 Angiogenesis involves multiple events in endothelial cells,including cell migration, proliferation and tube formation.Previously, we have demonstrated that VEGF activation of HIMECs resulted in cell migration, proliferation, tube and stressfibre formation.
25
To determine the antiangiogenic potential of curcumin and its potential mechanism of action through
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