e-mail:lixican@126.com;CDF27212@21cn.com
?
Bothauthorscontributedequallytothiswork
ANTIOXIDANTACTIVITYANDMECHANISMINFLOWEROF
HYLOCEREUSUNDATUS(HAW.)BRITT.ETROSE
XICANLI
1?
,YAOXIANGGAO
1?
,WEIJUANHAN
1
,JINGLIN
1
,QIUPINGHU
1
,
ANDDONGFENGCHEN
2
1
SchoolofChineseHerbalMedicine,
2
SchoolofBasicMedicalScience,
GuangzhouUniversityofChineseMedicine,Guangzhou,510006,China
ReceivedJanuary28,2013;revisionacceptedMay11,2013
HylocereusundatusfloweriscommonlyusedasfoodorformedicinalpurposesinsouthChina.Tostudyits
antioxidantactivityandmechanismweusedantioxidantandchemicalassaystocomparetwocommercialsam-
plesfromdifferentlocations(Shenjing,Qixing).Thedifferenceinantioxidantlevelscorrespondedwithdiffer-
encesinchemicalcontent(includingtotalphenolics,totalflavonoids,kaempferolandquercetin)between
ShenjingandQixing.TheantioxidantabilityofH.undatusflowerseemsattributabletototalphenolics(mainly
totalflavonoids).Kaempferolisoneofthemainbioactivecomponents.H.undatusflowerexertsitsantioxidant
effectsthroughmetalchelationandradicalscavengingviahydrogenatom(H?)andelectron(e)donation.
Keywords:Hylocereusundatusflower,antioxidantactivity,totalphenolics,totalflavonoids,
kaempferol,quercetin.
ACTABIOLOGICACRACOVIENSIASeriesBotanica55/1:80–85,2013
DOI:10.2478/abcsb-2013-00014
PLISSN0001-5296?PolishAcademyofSciencesandJagiellonianUniversity,Cracow2013
INTRODUCTION
Hylocereusundatus(Haw.)Britt.etRoseisaclimb-
ingvinecactusspecieswidelydistributedinmany
countriesincludingAustralia,Israel,Malaysia,
Nicaragua,Taiwan,Vietnam,andsouthChina.Its
flower(Fig.1)iscommonlyusedtopreparevarious
healthful,tastysoups.IntraditionalChinesemedicine
(TCM)thesesoupsarethoughttoexerteffectsinclud-
ingclearing"heat-fire,"moisturizingthelung,elimi-
natingphlegmandrelievingcough(Ye,1999;Zhou,
2001)PhytochemicalanalysesrevealedthatH.unda-
tusflowercontainsthreeglycosides(undatusidesA,
B,C)(Wuetal.,2011)andseveralflavonoids(Yietal.,
2012).Therearenoreportsonitsantioxidantactivi-
ty.Inthisstudyweinvestigateditsantioxidantactivi-
ty,andthemechanismofit,intwotypicalcommer-
cialsamplesofH.undatusflower,Shenjing
BawanghuaflowerandQixingJianhuaflower.
MATERIALSANDMETHODS
PLANTMATERIAL
ShenjingflowerisgrownonShenjingChangzhou
Island,Guangzhoucity,andthedriedShenjing
flowerwaspurchasedfromtheChangzhouveg-
etablemarket,Guangzhoucity,Guangdong
Province,China.Qixingfloweriswidelycultivated
inZhaoqingcityinGuangdongProvince,and
driedQixingflowerwasobtainedfromDinghutang
FoodProcessingFactory,GuangdongProvince,
China.Voucherspecimensaredepositedinour
laboratory.
CHEMICALS
DPPH?(1,1-diphenyl-2-picrylhydrazylradical),
ABTS[2,2''-azino-bis(3-ethylbenzo-thiazoline-6-sul-
fonicacid)diammoniumsalt],BHA(butylated
hydroxyanisole),Trolox[(±)-6-hydroxy-2,5,7,8-
tetramethylchromane-2-carboxylicacid],linoleic
acid,ferrozine[3-(2-pyridyl)-5,6-diphenyl-1,2,4-tri-
azine-p,p''-disulfonicacidmonosodiumsalt
hydrate],murexide(5,5''-nitrilodibarbituricacid
monoammoniumsalt),pyrogallolandFolin-
CiocalteureagentwerepurchasedfromSigma-
AldrichShanghaiTradingCo.,China.Kaempferol
andquercetinwereobtainedfromtheNational
InstitutefortheControlofPharmaceuticaland
BiologicalProducts(Beijing,China).Methanoland
waterwereHPLCgrade.Otherchemicalsusedin
thisstudywereanalyticgrade.
PREPARATIONOFEXTRACTS
ShenjingflowerandQixingflowerweresoakedin
70%ethanolatroomtemperatureforamonth,then
concentratedunderreducedpressuretoyieldSJFH
(ethanolextractofShenjingflower)andQXFH
(ethanolextractofQixingflower).Theywererefrig-
erateduntilusedforanalysis.
ANTI-LIPIDPEROXIDATION
Theanti-lipidperoxidationeffectwasinvestigatedin
linoleicacidemulsion(Lietal.,2009).Briefly,
1.5mLlinoleicacidemulsionwasmixedwith0.15mL
samplemethanolicsolution(0.4–2.0mg/mL)and
0.35mL30%ethanol(v/v).Thereactionmixture
(total2mL)wasincubatedatroomtemperaturefor
72h.Then0.15mLofthemixturewasaddedto
3.65mL75%ethanol(v/v),0.1mLNH
4
SCN(30%,
w/w),and0.1mLFeCl
2
(0.02Min3.6%HCl).
Absorptionat500nmwasmeasuredwithaUnico
2100spectrophotometer.Theinhibitionpercentage
wascalculatedbytheequation:
Inhibition%=(A
0
–A)/A
0
×100%
whereA
0
istheabsorbanceofthecontrolwithout
sample,andAistheabsorbanceofthereactionmix-
turewithsample.
?O
2
-
RADICALSCAVENGINGASSAY
Measurementofsuperoxideanion(?O
2
-
)scavenging
activitywasbasedonourmethod(Li,2012).In
brief,1mg/mLsampleethanolicsolution(×mL)
wasmixedwithTris-HClbuffer(2.92-×mL,0.05M,
pH7.4)containingEDTA(1mM).When80μLpyro-
gallol(60mMin1mMHCl)wasadded,themixture
wasshakenrapidlyat37°C.Theabsorbanceofthe
mixturewasmeasuredevery30sfor5minat
325nm.The?O
2
-
scavengingabilitywascalculated
usingtheformula(Li,2012):
Inhibition%=[(ΔA
325nm,control
/T)–
(Δ
A325nm,sample
/T)]/(ΔA
325nm,control
/T)×100%
Here,ΔA
325nm,control
istheincrementinA
325nm
ofthe
mixturewithoutthesampleandΔA
325nm,sample
is
thatwiththesample;T=5min.
Fe
2+
CHELATIONASSAY
Fe
2+
chelationactivitywasestimatedbythemethod
ofLietal.(2012a).Briefly,0.2mLsamplemethano-
licsolution(260–1040μg/mL)wasaddedto0.1mL
FeCl
2
aqueoussolution(250μM).Thereactionwas
initiatedbyadding150μLferrozineaqueoussolu-
tion(1mM)andthetotalvolumewasadjustedto
1.0mLwithmethanol.Thenthemixturewasshaken
vigorouslyandstoodatroomtemperaturefor10min.
Absorptionat562nmwasmeasuredspectrophoto-
metrically.Thechelationpercentagewascalculated
bytheformula(Lietal.,2012a):
Chelatingeffect%=(A
0
–A)/A
0
×100%
whereA
0
istheabsorbanceofthecontrolwithout
sample,andAistheabsorbanceofthereactionmix-
turewithsample.
Cu
2+
CHELATIONASSAY
TheCu
2+
chelationeffectwasanalyzedbythe
methodofLietal.(2012a).Briefly,0.06mLCuSO
4
aqueoussolution(20mM)wasaddedtohexamine-
HClbuffer(pH5.0,30mM)containing30mMKCl
and0.20mMmurexide.Afterincubationatroom
temperaturefor1min,0.030–0.18mLsample
methanolicsolution(13mg/mL)wasadded.The
finalvolumewasadjustedto1.5mLwithmethanol.
Thenthemixturewasshakenvigorouslyandleftat
roomtemperaturefor10min.Absorptionat
485nmand520nmwasmeasuredspectrophoto-
metrically.Theabsorbanceratio(A
485
/A
520
)reflected
thefreeCu
2+
content.Thecupricchelationpercent-
agewasthereforecalculatedastheequation(Liet
al.,2012a):
Chelatingeffect%=[(A
485
/A
520
)
max
–(A
485
/A
520
)]/
[(A
485
/A
520
)
max
–(A
485
/A
520
)
min
]×100%
where(A
485
/A
520
)istheabsorbanceratioofthesam-
ple,while(A
485
/A
520
)
max
isthemaximumabsorbance
ratioand(A
485
/A
520
)
min
istheminimumabsorbance
ratiointhetest.
AntioxidantactivityofHylocereusundatusflower
81
Fig.1.Hylocereusundatus(Haw.)Britt.etRoseandits
flower
DPPH?RADICALSCAVENGINGASSAY
DPPH?radicalscavengingactivitywasdetermined
asdescribed(Lietal.,2012a).Briefly,1mLDPPH?
ethanolicsolution(0.1mM)wasmixedwith0.5mL
sampleethanolicsolution(0.6–3.0mg/mL)andkept
atroomtemperaturefor30min.Thenabsorptionat
519nmwasmeasuredwithaspectrophotometer.
TheDPPH?inhibitionpercentagewascalculatedby
theformuladescribedin"ANTI-LIPIDPEROXIDA-
TION."
ABTS
+
?RADICALSCAVENGINGASSAY
ABTS
+
?scavengingactivitywasmeasuredas
describedbyLietal.(2012b).Briefly,1.2mLdilut-
edABTS
+
?reagentwasaddedto0.3mLsample
ethanolicsolution(0.08–0.4mg/mL).Afterincuba-
tionfor6min,absorbanceat734nmwasreadwith
aspectrophotometerandtheinhibitionpercentage
wascalculatedusingtheformuladescribedin
"ANTI-LIPIDPEROXIDATION."
CHEMICALANALYSIS
Totalphenolicscontentwasdeterminedusingthe
Folin-Ciocalteumethod(Lietal.,2012b).Briefly,
0.5mLsamplemethanolicsolution(1mg/mL)was
addedto0.5mLFolin-Ciocalteureagent(0.25M).
Themixturestoodfor3min,then1.0mLNa
2
CO
3
aqueoussolution(15%,w/w)wasadded.Afterincu-
bationatambienttemperaturefor30minthemix-
turewascentrifugedat3500rpmfor3min.The
absorptionofthesupernatantat760nmwasmeas-
uredwithaspectrophotometer.Thestandardcurve
waspreparedusingdifferentconcentrationsof
quercetinandtheresultwasexpressedasquercetin
equivalentinmilligramspergramextract.
Totalflavonoidcontentwasmeasuredusingthe
NaNO
2
-Al(NO
3
)
3
method(Lietal.,2012a).Briefly,
1mLsamplemethanolicsolution(10mg/mL)was
mixedwith0.15mLNaNO
2
aqueoussolution(5%,
w/w).Themixturestoodfor6min,followedbythe
additionof0.15mLAl(NO
3
)
3
aqueoussolution
(10%,w/w).Afterincubationforanother6min,
2mLNaOHaqueoussolution(4%,w/w)wasadded,
thenthemixturewasadjustedto5mLwithdistilled
water.Absorptionat508nmwasreadwithaspec-
trophotometer.Thestandardcurvewasobtained
usingstandardquercetinandtheresultwasalso
expressedasquercetinequivalentinmilligramsper
gramextract.
Kaempferolandquercetinwereidentifiedby
comparingtheirretentiontimesusingHPLC,per-
formedwithaSyltechP510system(LosAngeles,
CA,USA)equippedwithaDikmaDiamonsilC18
column(250mm×4.6mm,5μm)(Beijing,China).
Themobilephaseconsistedofmethanolandwater
(50:50,v/v),theflowratewas0.5mL/min,andthe
wavelengthwas360nm.Kaempferolandquercetin
contentintheextractswascalculatedonthebasisof
thecalibrationcurvesofkaempferolandquercetin
standards.
STATISTICALANALYSIS
Dataaregivenasmeans±SDofthreemeasure-
ments.TheIC
50
valueswerecalculatedbylinear
regressionanalysis.Alllinearregressionsinthis
paperusedOrigin6.0software.Thesignificanceof
differenceswascheckedwiththet-test(p<0.05)
usingSPSSsoftware(v.12,SPSS,USA).
RESULTSANDDISCUSSION
Underoxidativestress,unsaturatedfattyacidsmay
undergolipidperoxidation(LPO)andsubsequently
formreactivealdehydespeciesthatarebothcyto-
toxicandgenotoxicthroughtheirabilitytocovalent-
lymodifyproteinsandDNA(Sowelletal.,2004).
Manydiseasesareassociatedwithlipidperoxida-
tion,suchascardiovasculardisease(Halliwell,
2000),bronchitis(Ignatovaetal.,1998),protitis
(FilipenkoandSalii,2007),pulmonarytuberculosis
(Novitskiietal.,2005)andatherosclerosis(Sdvigova
etal.,1993).
Weusedalinoleicacidemulsionsystemto
assesstheanti-lipidperoxidationabilityofH.unda-
tusflower;bothSJFHandQXFHexhibitedanti-
lipidperoxidationactivityinaconcentration-
dependentmanner(Fig.2a).TheIC
50
valueswere
3.62±0.32μg/mLforSJFHand3.42±0.10μg/mL
forQXFH(Tab.1).ItsuggestedthatH.undatus
flowercaneffectivelypreventlipidperoxidation.
Lipidperoxidationmayoccurnonenzymatically
throughthereactionoflinoleicacidwithreactive
oxygenspecies(ROS)(Sowelletal.,2004).For
example,?O
2
-
,oneformofROS,candirectlydamage
lipidsoxidatively.Inaddition,?O
2
-
canfurthergen-
erate?OHradicalsviatheHaber-Weissreaction
(FangandZheng,2002).
Thehydroxylradical(?OH)withhighreactivity
canextract?Hfromlipid(LH)toproduceL?,LO?,
LOO?andLOOH.Therefore?O
2
-
scavengingiscon-
sideredtobeamechanismofpreventinglipidper-
oxidefromforming.BothSJFHandQXFHexhibit-
edstronger?O
2
-
radicalscavengingabilitythan
Troloxinthestudy(Tab.1),suggestingthat
H.undatusflowerexertedanti-lipidperoxidation
action,perhapsvia?O
2
-
scavenging.
Transitionmetals,especiallyFeandCu,playan
importantroleinROSgeneration.Weexaminedthe
metalchelationabilitiesofSJFHandQXFH.The
dose-responsecurvesconfirmedthatbothSJFH
Lietal.
82
AntioxidantactivityofHylocereusundatusflower
83
andQXFHpossessedeffectivemetalchelationabili-
ty(Fig.2c,d).Thechelationabilitycanbeattributed
mainlytopolyphenolsandespeciallyflavonoids(Li
etal.,2012a).Forexample,kaempferolisolated
fromH.undatusflower(Yietal.,2011)canbind
Cu
2+
via-OHandC=Ogroupsinorthopositions
(Torreggianietal.,2005).Metalchelationmaybe
anothermechanismtopreventLPO.
Tofurtherstudytheradicalscavengingmecha-
nism,SJFHandQXFHweresubjectedtoDPPHand
ABTSassays.Ourdatashowedthatbothextracts
effectivelyscavengeDPPH?andABTS
+
?radicals
IC
50
valueisdefinedastheconcentrationfor50%effect,calculatedbylinearregressionanalysisandexpressedasmeans±SD(n=3).
Meanswithdifferentsuperscriptsinthesamerowdiffersignificantlyatp<0.05.Thepositivecontrolissodiumcitrate.BHA–buty-
latedhydroxyanisole;SJFH–ethanolextractofShenjingflower,QXFH–ethanolextractofQixingflower,nd–notdetected.
Fig.2.Dose-responsecurvesofantioxidantassaysforSJFH,QXFHandpositivecontrols.SJFH–ethanolextractof
ShenjingBawanghuaflower;QXFH–ethanolextractofQixingJianhuaflower.(a)Anti-lipidperoxidation,(b)?O
2
-
radi-
calscavenging,(c)Fe
2+
chelationassay,(d)Cu
2+
chelationassay,(e)DPPH?radicalscavenging,(f)ABTS?
+
radicalscav-
enging.Valuesaremeans±SD(n=3).
TABLE1.IC
50
valuesforSJFH,QXFHandpositivecontrols(μg/mL)
Lietal.
84
(Fig.2e,f).PreviousresearchsuggestedthatDPPH?
maybescavengedbyanantioxidantthroughhydro-
genatom(H?)donationtoformastableDPPH-H
moleculethatdoesnotabsorbat519nm(Bondetet
al.,1997).Forexample,kaempferolcouldtransfer
H·toDPPH?andthentransformintoasemiquinone,
evenstablequinine(DimitriosandVassiliki,2006;
KhandujaandAnjana,2003).However,ABTS?
+
scavengingisconsideredanelectron(e)transfer
reaction(AliagaandLissi,1998).Thefactthatboth
SJFHandQXFHcaneffectivelyscavengeDPPH?and
ABTS?
+
suggeststhatH.undatusflowerexertsradi-
calscavengingactionbydonatinghydrogenatoms
(H?)andelectrons(e).
EarlierworksuggestedthatH.undatusflower
canbeusedasanadjuvanttherapyforatheroscle-
rosis(Liangetal.,1995),cardiovasculardiseases,
pulmonarytuberculosis,bronchitis,parotitis
(ZhonghuaBencao,2004)andotherconditions.
Thesepharmacologicaleffectsmayberelatedto
antioxidantaction(ZhengandHuang,2007).
WealsousedspectrophotometryandHPLCto
analyzethechemicalcontentofSJFHandQXFH,
includingtotalphenolics,totalflavonoids,
kaempferolandquercetin.AsseeninTable2,the
chemicalcontentofSJFHwasgenerallylowerthan
thatofQXFH.Thedifferenceinchemicalcontent
paralleledthedifferenceintheirantioxidantlevels.
Itcanbeinferredthattheantioxidantabilityof
H.undatusflowerisattributabletoitschemical
components.Thisconclusionisexpected,assimilar
observationshavebeenreported(Lietal.,2009).
Totalphenolicsincludeflavonoids,phenolicacids,
tannins,anthocyaninsandothers.Inourstudythe
highratiosoftotalflavonoidsversustotalphenolics
(10.34:25.27forSJFHand21.28:53.34forQXFH)
suggestthatflavonoidsarethemainformoftotal
phenolics(Tab.2),sotheantioxidantabilityof
H.undatusflowerseemsmainlytheeffectof
flavonoids.Thirteenflavonoidshavebeenisolated
fromH.undatusflower,includingkaempferol,
quercetin,isorhamnetinandothers(Yietal.,2011).
Ourresultsindicatethatkaempferolcontentwas
muchhigherthanquercetincontent(Tab.2,Fig.3);
kaempferolisoneofthemainbioactiveantioxidant
componentsofH.undatusflower.
CONCLUSIONS
Asanedibleormedicinalplantmaterial,H.undatus
flowerhasantioxidanteffects.Itsantioxidantaction
isduemainlytoitscontentoftotalflavonoids,
amongwhichkaempferolisaprincipalbioactive
component.Itexertsitsantioxidanteffectthrough
metalchelation,andradicalscavengingviahydrogen
atom(H?)andelectron(e)donation.
ACKNOWLEDGMENTS
Wethanktheanonymousreviewerforvaluablecom-
mentsandsuggestions.Thisworkwassupportedby
theNationalNatureScienceFoundationofChina
(81273896)andtheNationalKeyTechnologiesR&D
ProgramofChina(No.2008BAI51B01).
TABLE2.ChemicalcontentofSJFHandQXFH
Valuesaremeans±SD(n=3).Valueswithdifferentsuperscripts
inthesamerowdiffersignificantlyatp<0.05.SJFH–ethanol
extractofShenjingflower,QXFH–ethanolextractofQixing
flower.Expressedasmgquercetin/gextract.
Fig.3.HPLCchromatogramofstandards(a)andtypical
HPLCprofileofextractfromflowerofHylocereusunda-
tus(Haw.)Britt.etRose(b).SyltechP510system(Los
Angeles,California,USA),DikmaDiamonsilC18column
(250mm×4.6mm,5μm)(Beijing,China),methanol-
water(50:50,v/v)mobilephase,0.5mL/minflowrate,
360nmwavelength.
AntioxidantactivityofHylocereusundatusflower
85
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