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Starch materials as biocompatible supports and procedure for fast separation of macrophages

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Tiêu đề Starch Materials as Biocompatible Supports and Procedure for Fast Separation of Macrophages
Tác giả Khalil Sakeer, Tatiana Scorza, Hugo Romero, Pompilia Ispas-Szabo, Mircea Alexandru Mateescu
Trường học Université du Québec à Montréal
Chuyên ngành Biochemistry and Biomedical Sciences
Thể loại Research Article
Năm xuất bản 2017
Thành phố Montreal
Định dạng
Số trang 10
Dung lượng 4,12 MB

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Nội dung

Different starch derivatives were evaluated as supports for attachment and recovery of macrophages (RAW 264.7 line). Gelatinized starch (G-St), acetate starch (Ac-St), carboxymethyl starch and aminoethyl starch were synthesized and characterized by FTIR, 1H NMR, SEM and static water contact angle.

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jo u r n al h om ep age :w w w e l s e v i e r c o m / l o c a t e / c a r b p o l

Khalil Sakeera, Tatiana Scorzab, Hugo Romerob, Pompilia Ispas-Szaboa,

Mircea Alexandru Mateescua,∗

a r t i c l e i n f o

Keywords:

Alpha-amylase

a b s t r a c t

Differentstarchderivativeswereevaluatedassupportsforattachmentandrecoveryofmacrophages (RAW264.7line).Gelatinizedstarch(G-St),acetatestarch(Ac-St),carboxymethylstarchandaminoethyl starchweresynthesizedandcharacterizedbyFTIR,1HNMR,SEMandstaticwatercontactangle.These polymersarefilmogenicandmaycoatwelltheholderdevicesusedformacrophageadhesion.Theyalso presentasusceptibilitytomildhydrolysiswithalpha-amylase,liberatingtheadheredmacrophages Cellcounts,percentageofdeadcellsandleveloftumornecrosisfactor(TNF-␣)wereusedtoevaluatethe possibleinteractionbetweenmacrophagesandstarchfilms.Thehighpercentageofcelladhesion(90–95%

onG-StandonAc-St)associatedwithenzymaticdetachmentofmacrophagesfromfilm-coatedinserts, resultedinhigherviabilitiescomparedwiththoseobtainedwithcellsdetachedbycurrentmethods scrappingorvortex.Thisnovelmethodallowsafastmacrophageseparation,withexcellentyieldsand highviabilityofrecoveredcells

©2017TheAuthor(s).PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBYlicense

(http://creativecommons.org/licenses/by/4.0/)

1 Introduction

Starch is widely used in food, pharmaceutical and

biomed-ical applications due to its biocompatibility, biodegradability,

non-toxicity and abundant sources (Rowe, Sheskey, Cook, &

Fenton,2009).Starchmodificationisgenerallyachievedthrough

derivatizationsuchascross-linking(Lenaertsetal.,1998),

etherifi-cation,esterification(Calinescu,Mulhbacher,Nadeau,Fairbrother,

&Mateescu,2005;Mulhbacher,Ispas-Szabo,Lenaerts,&Mateescu,

2001)andgrafting(Kaur,Singh,&Liu,2007)offunctionalgroups

onto the carbohydrate structure Such modifications can

pro-foundlyalterthephysicochemical andmorphologicalproperties

ofstarch,itsenzymaticdigestibilityandcanconsequently

mod-ulateitscurrent useasexcipientin drugdeliverydosageforms

(Mulhbacher,Ispas-Szabo,&Mateescu,2004;Massicotte,Baille,&

Mateescu,2008).Aninterestingreportedapplicationofstarchwas

itsuseforenrichmentofmacrophagecellpopulationsby

adhe-siononcross-linkedstarchmicrospheresfollowedbyliquefaction

ofmicrobeadswithalpha-amylase(Desmangles,Flipo,Fournier,&

Mateescu,1992).Macrophagesarecurrentlyinvestigatedin

iousbiochemicalandbiomedicalfieldsaswellasfortherapeutic applications (Kwan, Wu, &Chadban, 2014; Ostuni, Kratochvill, Murray,&Natoli,2015;Wooden&Ciborowski,2014;Youetal.,

2013).Macrophageswithapossibleroleininflammatoryprocesses andmalignancywerereportedasanewtherapeutictarget.There

isagrowinginterestfortechniquesofmacrophageseparation, par-ticularlytoinvestigateanti-macrophagesnovelstrategiesagainst cancer.Macrophagescanbeobtainedinarelativelypureformas primaryculturesforanalyticalandbiochemicalmanipulationsbut theydo notgenerallyreplicateinculture,haverelatively short-lives, and maybe difficultto obtainenough amounts for large scale.Theyareverysensitivetosmallchangesintheir environ-ment andmay bedamaged considerably,even when delicately handledaftercellculture(Adams,1979;Féréoletal.,2006) Detach-ingadherentmacrophagesfroma culturedish isdifficult,since thesecellsadhereavidlytoplasticsurfacesofcellculturedevices (i.e.Petri dishes,microplates) Severalprocedures arecurrently appliedtoregainmacrophagesuchasmechanicaldetachmentby gentlescrapingof macrophageswitha rubberpoliceman(Fleit, Fleit,&Zolla-Pazner,1984;Jaguin,Houlbert,Fardel,&Lecureur,

2013;Porcherayetal.,2005)orpre-treatmentwithscandicainK, proteinase,orpronase(Malorny,Neumann,&Sorg,1981),whichis limitativeasithasmitogeniceffectsonmacrophages.Frequently

bymechanicaldetachment,abouthalfofcellsmayremainviable

http://dx.doi.org/10.1016/j.carbpol.2017.01.053

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ofviablecellsaremajorlimitationsforexistingprocedures

Based onourpreviousseparation of macrophages by

reten-tiononacross-linkedstarchcolumnandfurtherdetachmentby

enzymatichydrolysisofthechromatographicsupport(Desmangles

etal.,1992),fourstarchmaterialsnamelygelatinizedstarch

(G-St), acetate starch (Ac-St), carboxymethyl starch (CM-St) and

aminoethylstarch (AE-St)were investigatedfor their abilityto

formfilmssusceptibletoamylolysistobeusedassubstrate/support

for macrophage separation by mild enzymatic amylolysis.This

approachisdifferenttothepreviousreportedmethod(Desmangles

etal.,1992)toseparatemacrophagesusingcross-linkedstarchas

achromatographicsupport.Ingeneral,cross-linkedmaterialsare

adequatetoformmicrospheresbutpresentlowerfilmogenicability

thantheuncross-linkedmaterials(Berezkin&Kudryavtsev,2015;

Krumova,López,Benavente,Mijangos,&Pere ˜na,2000).Amajor

objectiveofthisstudywastounderstandthecriticalroleofsurface

propertiesofstarchmaterialsontheattachmentofmacrophages

andconsequentlytheinfluencesontheirviability

2 Materials and methods

2.1 Materials

High amylose starch (Hylon VII) was supplied by National

Starch (Bridgewater, NJ, USA) Sodium monochloroacetic acid,

3,5-Dinitrosalicylicacid, sodiumpotassiumtartratetetrahydrate

(Sigma-Aldrich, Germany), d-(+)-Maltose monohydrate

(Sigma-Aldrich, Japan), amyloglucosidase (EC 3.2.1.3) from Aspergillus

niger ≥300U/mL (Sigma-Aldrich, Denmark), acetic anhydride

(Anachemia,Montreal,Canada),␣-amylase(EC3.2.1.1)from

Bacil-lus subtilis 402U/mg (Fluka, Switzerland), 2-chloroethylamine

hydrochloride (Fluka, Switzerland) were all used as received

without further purification CellTrackerTM Green CMFDA

(5-chloromethylfluoresceindiacetate)andpropidiumiodide

(Invitro-gen,UK),lipopolysaccharide(LPS,L3012,Sigma-Aldrich),TNFELISA

kitsfromBiolegend(San Diego,CA)were usedformacrophage

cellscharacterization.TheRAWmacrophagecells(ATCCTIB-71)

wereculturedinRPMI-1640mediumsupplementedwith10%fetal

bovineserumandantibiotics(PenicillinandStreptomycin)

Sub-cultureswerepreparedbygentlescrappingandaspirationpriorto

testinginstarchcoatedsupports

2.2 Preparationofstarchfilmogenicmaterials

Anamountof12.50gofHylonVIIwassuspendedforhydration

in 50mLof distilled water at60–70◦C under continuous

verti-cal stirring (ServodyneMixer, 50000-40, IL, USA) A volume of

75mLof5MNaOHwasaddedtothestarchsuspension,

contin-uing thestirringfor 60minat60–70◦C Thenthesolutionwas

cooleddown and neutralized withglacial acetic acid(untilpH

6.8)togetgelatinized starch (G-St).Thegelatinized starchwas

furtherderivatized either bydirect addition of 18.75mL acetic

anhydride,or byadditionof 18.75gsodiummonochloroacetate

or2-chloroethylaminehydrochloride(eachsolubilizedina

min-imalwatervolume)understirringandcontinuingthereactionfor

1hat60–70◦Ctoobtainacetate(Ac-St),carboxymethyl(CM-St),

oraminoethyl(AE-St)starchderivatives,respectively.Then,each

solutionwascooleddownandneutralizedwithglacialaceticacid

(toreachpH6.8).Thederivatizedstarchpowderswereobtainedby

precipitationfromthereactionsolutionwithanequivalentvolume

ofmethanol/water(70:30)v/vsolution.Forallstarchmaterials,the

processwasrepeateduntilafinalconductivityoffiltratedecreased

atabout50␮S/cm.Then,200mLofmethanol100%wereused,

fol-lowedby200mLofacetone100%forfinaldrying.Thecollected

powderswereleftatroomtemperatureforcompleteairdrying overnightandsievedtoobtainparticlesoflessthan300␮m 2.3 Evaluationofsubstitutiondegreeofderivatives

FortheCM-StandtheAE-St:thedegreeofsubstitution(DS) wasdeterminedbyback-titrationaspreviouslydescribed(Assaad, Wang,Zhu,&Mateescu,2011; Stojanovi ´c,Jeremi ´c, Jovanovi ´c,& Lechner, 2005) Briefly, 100mg of polymer were solubilized in

10mLof0.05MNaOHandthentheexcessofNaOHwastitrated (n=3)with0.05MHCl usingphenolphthalein asindicator The blank(20mLof0.05MNaOH)wasalsotitratedbythesamemethod ThedegreeofsubstitutionofAc-Stwasdeterminedtitrimetrically, followingthemethodofSodhiandSingh(2005)withminor mod-ifications.Acetylatedstarch(0.1g)wasplacedina25mLflaskand

6mLofDimethylsulfoxide(DMSO)wereadded.Theloosely stop-perflaskwasagitated,warmedto50◦Cfor30min,cooleddownand then4mLof0.05MKOHwereadded.Thealkaliexcesswas back-titratedwith0.05MHClusingphenolphthaleinasanindicator.The amountsof COOH, NH2and COCH3 groupsandtheDSwere calculated(Stojanovi ´cetal.,2005)usingthefollowingequations:

whereVb(mL)isthevolumeofHClusedforthetitrationofthe blank;V(mL)isthevolumeofHClusedforthetitrationofthe sam-ple;CHClistheconcentrationofHCl;162(g/mol)isthemolecular massofglucoseunit;W=(58or44or43)(g/mol)istheincreasein themassofglucoseunitbysubstitutionwithonecarboxymethyl, aminoethylandacetylgrouprespectively,andm(g)isthemassof drysample

2.4 Fouriertransforminfrared(FT-IR)analysis TheFT-IR spectraofsamplesas powderswererecorded(64 scansata4cm−1resolution)usingaThermo-Nicolet6700 (Madi-son, WI, USA) FT-IR spectrometer equipped with a deuterated triglycinesulfate-KBr(DTGS-KBr)detectorandadiamondsmart ATR(attenuatedtotalreflection)platform

2.5 1HNMRmeasurements The1HNMRspectrawerecollectedusingahigh-field600MHz BrukerAvanceIIIHDspectrometerrunningTopSpin3.2software and equipped with a 5mm TCI cryoprobe The temperature of sampleswasmaintainedat27◦C.Thesamplesweredissolvedin deuterateddimethylsulfoxide-d6 (DMSO-d6) withboth methyl groupsdeuterated,thenheatedat65◦Cfor30min,andkeptat4◦C for2h

2.6 Scanningelectronmicroscopy(SEM) Themorphologyoftheparticlesandfilmsurfacewereexamined

byaHitachi(S-4300SE/N)scanningelectronmicroscopewith vari-ablepressure(HitachiHighTechnologiesAmerica,Pleasanton,CA, USA)at5–7kVandmagnificationsof100and1000×forpowders andof500×and1000×forfilmsurface.Samplesweremountedon metalstubsandsputter-coatedwithgold

2.7 Filmcastingandmacrophageculture 2.7.1 Preparationoffilm-formingsolutionsofstarchmaterials Gelatinizedstarch(G-St),acetatestarch(Ac-St),carboxymethyl starch(CM-St)andaminoethylstarch(AE-St)havebeendispersed

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Scheme 1.Design of device and procedure with adhesion (1) and amylolysis (2) steps for fast recovery of macrophages.

at0.5%(w/v)inpurifiedwaterandheatedto95◦C.Thenthe

solu-tionswerecooleddowntoroomtemperatureandcentrifugedat

5000rpmfor2min.Foreachfilmformingmaterialthesupernatant

wascastonacellcultureinsertdevicewithabasefilterof

polyethy-leneterephthalate(PET)having3.0␮mporeaperture(BDFalcon

CellCultureInserts,353092,USA).Thesolutionwasevaporatedat

40◦Cfor12htoformthefilmcoatingoftheinsertdevice

2.7.2 Macrophageincubation

Beforeincubation theinsertand plates(Costar® 35166well

plate,USA)weresterilizedbyUV-rayfor15min.Then,macrophage

suspensionsinaRPMI-1640culturemediumcontainingFBS10%

andPenicillin/Streptomycin1x,wereincubatedfor48hina

humid-ifiedatmosphereofairand5%CO2at37◦C.Theculturemediumwas

introducedfromtheoutsideofcellcultureinsert(Scheme1)

2.7.3 Microscopy

Themorphology of macrophage cells was investigated after

incubationfor48hontothecellcultureinsertcoatedwithG-St,

CM-St,Ac-StorAE-St.Macrophageswerelabeledwithfluorescent

stainingCellTrackerTMGreenCMFDAandpropidiumiodide

follow-ingmanufacturerinstructions.CellswerevisualizedusingaNikon

EclipseTimicroscope(NikonCanada,Mississauga,ON)equipped

withphasecontrastandepifluorescenceoptics.Photomicrographs wereacquiredusing aDigital SightDS-Qi1Mccamera and NIS-Elements3.0software(NikonCanada)

2.7.4 Susceptibilitytoenzymatichydrolysisofstarchfilms Thefilmhydrolysiswasdoneinthreesteps:(a)Hydration step:

Culturemediumwasreplacedby40mMphosphatebufferpH7.4

at37◦Cinsideandoutsideofeachcellcultureinsert;(b) Liquefac-tion step:Asolutionofanalpha-amylase(EC3.2.1.1fromBacillus subtilis)in40mMphosphatebufferpH7.4(1000U/mL)wasused forliquefactionoffilmlayer.(c)Saccharification step:A40mM phosphatebufferpH7.4wasusedtodiluteamyloglucosidasefrom Aspergillusnigerupto(100U/mL)andthenusedfor saccharifica-tionofthestarchfilmspicesresultedfrompartialhydrolysiswith alpha-amylaseundergentleshakingfollowedbyincubationina humidifiedatmosphereofairand5%CO2 at37◦C(Aneja,2009; Lareoetal.,2013)

2.7.5 Determinationofenzymaticactivityonthestarch filmogenicsupports

Enzymaticactivityofalpha-amylasewasmeasuredonthesame filmamylolysisconditionsusingthedinitrosalicylic(DNS)method (Bernfeld,1955)tomeasurethereducingsugargroupsreleasedas

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Fig 2. 1H NMR spectra of Gelatinized starch (Red), Acetate starch (Green), Carboxymethyl starch (Blue) and Amino-Ethyl starch (Black).

resultofalpha1,4glycosidicgrouphydrolysis.Atdifferenttime

points a hydrolyzedsolution volumeof 0.5mLwaswithdrawn

immediately0.5mLofDNSreagentwasaddedtostopthe

hydrol-ysisreaction.Then,thereactionmediawereboiledfor 5minto

developthecolorofreduced3-amino-5-nitrosalicylicacid

Sub-sequently,after5minpreciselythesolutionswerecooledinan

ice-bathtoroomtemperatureand1mLofeach cooledsolution

wasdilutedwith4mLofdistilled water.Theabsorbanceofthe

finalsolutionafterfiltrationwasmeasuredagainstablank

solu-tionwithoutfilmogenicmaterialat540nm.Maltosesolutionswere

used(asstandardreducingsugar)togenerateastandardcurve.The

requiredtimeforfilmhydrolysiswasobservedvisually

2.7.6 Macrophagecellrecoveryandcounting

Macrophages current recovery approach was the scratching

procedure(usedascontrol)andtherecoverybythenoveldirect

collectionfromstarchcoatedinsertsdevicesafterthemild

enzy-matic filmhydrolysis were compared bycountingdone witha

hemacytometer(NikonTMS-F),andusingTrypanblueasstaining

agent

2.7.7 Macrophageactivation

Follwoing48hincubationanamountof 50ng/50␮LLPSper

1mLofculturemediumwasaddedandthecellsre-incubatedfor

additional72h

2.7.8 Quantitationoftumornecrosisfactor(TNF-˛)

After 72h incubation, the culture medium over and under

of macrophage layer was gently removed and centrifuged at

12000rpmfor 10min.The amountofTNF-␣wasquantifiedby

theELISAkit (CatalogueNo 430904,Biolegend,Canada) TNF-␣

levelinsamplesweredeterminedaccordingtothemanufacturer’s

instructions Astandardcurvein concentrationsfrom7.8pg/mL

to 125pg/mL was donein duplicate and the level of TNF-␣in thesupernatantswasevaluatedbyuseofthestandardcurveas reference The opticaldensity at 450nm wasmeasured witha microplatereader

2.8 Statisticalanalysis Alltestswereperformedintriplicateanddataarereportedas means±SD.Statisticalanalysisofdatawasperformedusingone wayANOVA,followedbyFisher’sposthoctestswithaminimum confidencelevel(P<0.05)forstatisticalsignificance

0 20 40 60 80 100 120

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3 Results and discussions

3.1 Polymerandfilmcharacterization

Thedegreeofsubstitutionof starchderivativesCM-St, Ac-St

andAE-St,asdeterminedbyback-titrationwereabout0.018,0.022

and0.024,respectively.Thesevaluesrepresenttheaveragenumber

ofcarboxymethyl,acetateoraminoethylgroupsperglucoseunit,

respectively.Thegraftingofeachfunctionalgrouponthestarch

chainswasconfirmedbystructuralanalysis,FT-IRand1HNMR

TheFourier transforminfrared (FT-IR)spectraoftheobtained

starchmaterials(Fig.1)presentabroadbandat3200–3300cm−1

duetothestretchingvibrationsof OH.Smallbandsat2927cm−1

andat2323cm−1attributedtothe−CHstretchingvibrationanda bandat1079cm−1ascribedto CH2 O CH2stretchingvibrations (Ispas-Szabo,Ravenelle,Hassan,Preda,&Mateescu,1999).Incase

ofCM-St,thereareadditionalbandsat1589cm−1andat1323cm−1 ascribedtoCOO−group(Friciu,TienLe,Ispas-Szabo,&Mateescu,

2013).Thehighintensityofthebandat999cm−1forAE-Stcould

beascribedtoC Nstretchingvibrations,whereastheweak shoul-derataround1735cm−1couldbeassignedto NH3 group(Assaad

etal.,2011;Deng,Jia,Zhang,Yan,&Hou,2006).InthecaseofAc-St, theweakshoulderataround1556cm−1correspondsspecificallyto the C Ostretchingofacetylgroups(Bello-Pérez,Agama-Acevedo, Zamudio-Flores,Mendez-Montealvo,&Rodriguez-Ambriz,2010;

Colthup,Daly,&Wiberley,1990)

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Fig 5.Scanning electron microscopy micrographs of films: Gelatinized starch (G-St), (b) Acetate starch, (Ac-St), (c) Carboxymethyl starch (CM-St) and (d) Amino-Ethyl starch

The 1H NMR spectraof the starch materials(Fig.2) present

protonsignalsat5.3ppmforH1andat3.3–3.9ppmforH2-6on

thestarchbackbone(Yangetal.,2014)whilethepeakat5.6ppm

canbeassignedtoOH3.ThemostsignificantpeaksforAE-Stare

at␦=4.15–4.25,␦=3.16–3.18,whichbelongtothehydrogensof

aminoethylgroup.IncaseofAc-Stthepeaksat␦=1.9–2.1andat

␦=3.5ppmareascribedtomethylprotonsofacetategroups(Xu

andHanna,2005).IncaseofCM-Stsharplesspeaksmaybedueto

thelimitedsolubilityofCM-StinDMSO

Theobtainedzetapotential(␨)chargesvaluesinsolutionwere

−32mVforG-Stand−38mVforCM-St.Thesevaluesareconsistent

withthechemicalmodificationofstarchbycarboxymethylgroups

providingastrongernegativecharge(Wongsagonsup,Shobsngob,

Oonkhanond, & Varavinit, 2005a; Wongsagonsup, Shobsngob,

Oonkhanond, & Varavinit,2005b) Grafting starch with acetate

groups reducedthevalueofzetapotentialforacetatestarch to

−26mV and this can be explained by a decreased polarity in comparisonwithG-St.ThepositivezetapotentialvalueforAE-St +10mVisrelatedtocationicgroupsgraftedonstarchmolecules StaticwatercontactangleFig.3allowedtheevaluationofthe wettability/hydrophilicity of the filmsfor coating of the insert surfaces The CM-St and AE-St films presented a lower angle (67◦ and78◦respectively)incomparisontoG-St(89◦)andAc-St (105◦),meaningthatG-StandAc-Starelesspolarandevenmore hydrophobic

Scanningelectronmicroscopy(SEM)ofstarchmaterialsas pow-dersandfilmsarepresentedinFig.4.Thenativestarch(Hylon VII)hasagranularaspectpredominantlyroundorovalinshape (Fig.4 withsmoothsurfaceanduniformrangeofsizedistribution (5–10␮m).Thegranularaspectfitswellwiththeknowncrystalline

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Fig 6. Confocal fluorescence microscopy images showing live cells (green) and dead macrophage cells (red) after incubation 48 h on cell inserts coated with Amino-Ethyl

structureofnativestarch(Friciuetal.,2013)stabilizedby

hydro-genbondsbetweenthehydroxylgroupsofglucopyranoseunits

Theaspectofthefourmaterials:G-St,CM-St,AE-StandofAc-Stis

different,dependingonmodificationoperatedonstarchstructure

TheG-St(Fig.4a)showedaroundandsponge-likeshapewhich

isduetothephysicalmodification(gelatinization)ofnativestarch

Differently,theCM-St(Fig.4b)presentedanirregularshapewith

anunevensurfacelikelyduetotheassociationofnumeroussmall

particlesforminglargergranulessimilarshapeswereobtainedby

Friciuetal.(2013).Thecarboxylicgroupsmayreducethenetwork

self-assemblingbyhydrogenassociationbetweenhydroxylgroups

andpromoterepulsioneffectsloadingtoastructural

reorganiza-tion(Lemieux,Gosselin,&Mateescu,2010).Theacetylation(Fig.4c)

generated a slightly roughsurface of granules which appeared

fusedinakindofaggregate.Theacetylgroupscanalsodecreasethe

starchstabilizationbyhydrogenbondingand,atthesametime,the

glucoseunitswithpolarhydroxylicgroupsandnon-polar(acetate)

functions,mayfavorstarchmacromoleculestocoalescetogether

resultinginakindoffusionofgranules(Bello-Pérezetal.,2010;

Singh,Kaur,&Singh,2004).TheAE-St(Fig.4d)grainsshoweda porousirregularshape,whereaminegroupsmaypromote hydro-genbondingresultingtoareorganizationoftheAE-Stnetwork.As farasfilmsareconcernedtheSEMmicrographsofG-StandCM-St filmsatmagnificationsof500×and1000×(Fig.5aandb)showeda homogeneousandsmoothsurface,whereasAc-StandAE-Stfilms (Fig.5candd)showedcontinuousmatrices,withsmallcracksand lesssmoothsurface

3.2 Macrophagecellsattachmentandrecoverybyfilmamylolysis 3.2.1 Morphologyofmacrophagecells

Intact macrophage cultures were treated with two staining agents:CMFDAtoshowlivecells (green)and propidiumiodide

tostaindeadcellswithalteredmembranepermeability(red) Controlculturesonuncoatedinsertdevices appearasplump

orstellate,monolayersroundedandspindle-likewithmajorityof

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0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 2

Time (min)

0 10 20 30 40 50

0 5 10 15 20 25 30 35 40

5)

0 10 20 30 40 50 60 70 80 90 100

livecells.Macrophagesincubatedoninsertdevicescoatedwith

G-St,Ac-StandAE-Stshowedround,compactandmostlylivecells

Fig.6.Differently,prevalentlydeadcellswereobservedwhen

incu-batedininsertcoatedbyCM-Stfilm,owninground,spindle-like

andtranslucentcytoplasm.Thisbehavioursuggeststhatthe

car-boxymethylfunctionalizedfilmmaycausemembranedisruption

and cell apoptosis.Similar damaged membranes and apoptosis

havebeenobservedwithcertainagentssuchascarboxy-silicalite

(Petushkov,Intra,Graham,Larsen,&Salem,2009)

3.2.2 Determinationofenzymaticactivitywithstarchfilmogenic

supportsassubstrates

Thefilmamylolysisprocesswasinvestigatedbymeasuringthe

enzymaticactivityofalpha-amylasewithvariousfilmsassubstrate

(Fig.7A).ItwasfoundthatG-St,AC-StandAE-Stshowedsimilarfilm

hydrolysisrateoverthefirst40min.Then,theG-sthydrolysiswas

fasterthanthatofAC-StandAE-St.Thisbehaviourwasconsidered

asnormalbecausethereisnochemicalmodificationoftheG-St

ThelowestenzymaticactivitywasobservedwithCM-Stfilm,where

thereleasedamountofmaltoseafter75minwasalmosthalfofthat

liberatedfromG-St.Thefilmhydrolysiswasalsofollowedvisually

Evenwithoutcompleteamylolysis,theCM-Stfilmwasdissolved

inlessthan10min,becauseCM-Stissolubleinalkalinemedium

Differently,G-St filmwaspartially hydrolyzedin 30min,AC-St

andAE-Stin40min.Macrophagesadhereonadequatesurfaces

and floatingcells arecharacteristically dying cells Macrophage countingsuggestedgoodadhesiononG-St,onAc-StandonAE-St materials.Fig.7Bpresentsthenon-adherent(floating)fractionof macrophagesafterincubationofcellcultureoncell-holderdevices (insert)coatedwithCM-St,AE-St,Ac-StorG-St.thehigher per-centagesofdeadmacrophage(floating)wereobservedatinserts coatedwithanionic CM-St(about 32±5%)orwiththecationic AE-St(about32±9%),whereasalowpercentageofdeadcellwas observedwithinsertcoatedwithnon-ionicandneutralpolymers Ac-St (5±2%) and G-St (9±3%)respectively, suggesting higher percentageoflivingcellsfromthisfilms.Theseadhesiondataon non-ionicAc-StandG-Stareinagreementwithourpreviousreport showinggoodadhesionandrecoverybyamylolysisofmacrophage cellsoncross-linkedstarchmicrospheres,notmodifiedwithionic groups(Desmanglesetal.,1992).ThebestretentiononAC-Stfits wellwith a studyof Godek, Michel,Chamberlain, Castner, and Grainger(2009),showingthatmacrophagesadherepreferentially

tohighlyhydrophobicfluorinatedsurfaces(Godeketal.,2009) Similarresults,butnotoncarbohydratematerials,wereobserved

byBrodbecketal.(2002)showingthatthehydrophilicandanionic polyethyleneterephthalatemodifiedsurfacesinhibitadhesionof monocyteandmacrophagecells(Brodbecketal.,2002)

Duetomembranedisruptionandcellinducingapoptosisalong withlowmacrophageviabilityonCM-St,thissupportwasexcluded fromfurtherinvestigationandcellharvestingandcountingwas

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AE-Stcoated inserts.Cell harvestingwasdoneby scrappingfor

controlcells (culturedon uncoatedinsert devices) or by

enzy-matic hydrolysis for insertscoated withstarch materials.After

incubationfor 48h, cell numbersincreasedabout 3.2times for

controluncoatedinserts,4.2timesforAc-Stand5.3timesfor

G-Stwhereasonly1.5timeswasobservedforAE-Stcoatedinsert

(Fig.7C).Furthermore,129%and164%morecellswererecovered

frominsertsdevicescoatedwithG-StandAc-Stwhencompared

tocontrols(un-coatedinserts),whereasa53%dropoftheyield

wasobtainedforAE-Stcoatedinserts.Thisinhibitoryeffectcould

beexplainedbya toostronginteractionofcationicaminoethyl

groupsofstarchfilmwithmembranephospholipidsofmacrophage

cells (Kurtz-Chalot et al., 2014) Therefore the AE-St was not

retainedforfurtherinvestigation

Macrophage activation by Lipopolysaccharide (LPS) and

quan-titation of induced tumor necrosis factor (TNF-a) allowed the

investigation of the possible effect of starch derivatives with

macrophageactivities.ThecellswerestimulatedwithLPS,a

com-ponentoftheoutermembraneofGramnegativebacteria,which

isapotentactivatorofmonocytesandmacrophages(Mace,Ehrke,

Hori,Maccubbin,&Mihich,1988).LPStriggerstheabundant

secre-tionofcytokinesbymacrophagesincludingtumornecrosisfactor

(TNF-a), interleukin (IL)-1, and IL-6 (Meng & Lowell, 1997) In

our study, the amount of TNF-␣ secreted by macrophages in

responsetoLPSwasinthesamerange asreportedin asimilar

study(Lichtman,Wang,&Lemasters,1998).Moreover,therewere

nodifferences(Fig.7D)inTNF-␣producedbycontrolcells

har-vestedfromuncoatedinserts(91±3.5pg/mL)orbymacrophages

harvestedfromG-St (90±2.3pg/mL)and Ac-St(89±2.9pg/mL)

coatedinserts.Thefunctional groups graftedonpolysaccharide

chainsnotonlyhaveadirecteffectonviabilityofcells,butthey

canimpactmacrophageadhesion.Forinstancethenon-derivatized

starch(G-St)andtheAc-Stwithhydrophobicacetategroups

ori-entedtoward culturemedium,arebettersupportsforadhesion

ofmacrophagecellsthantheanionic(CM-St)andcationic(AE-St)

starchderivativeswhicharelesscompatible.Theminimal

percent-ageofdeadcells(non-adherentfraction)wasobservedwithinserts

coatedwithG-StandAc-St.Therefore,theseGelatinizedstarchand

Acetatestarchmaterialsaffordingabestviability,couldbeagood

choiceassupportmaterialformacrophagecultureduetothehigh

compatibilitywithcells andalsofortheirsusceptibilitytomild

enzymaticamylolysis.ThesefeaturesofG-StandAc-Stallowthe

recoveryofmacrophagecellswithbetterviabilityandhighyields

Furthermore,theactivationbyLPSindicatedthatmacrophagecells

culturedonG-Standonthestarchacetatederivativeare

produc-ingalmostthesamelevelofTNF-␣asthecontrol(uncoatedinsert)

Thisresulttogetherwiththelowpercentageofdeadcellscould

beanevidenceofbiocompatibilityofG-StandAc-Stsupportsas

materialsformacrophagepreparationbythisnovelmildenzymatic

procedure

4 Conclusion

Thepresent studyisproposinganewtypeofapplicationfor

modifiedstarchbasedonitsfilm-formingcapacity.Theproposed

approach,focusedonadhesionofmacrophagecells onAc-St or

G-Stfilms followed bytheirdetachment by enzymatic

amylol-ysis,is faster and the mild condition affords a better viability

ofmacrophagecellsincomparison withtheclassicalprocedure

(mechanicaldetachment).Starchfilmsareeasy toapplyonthe

insertsand theirbiocompatibilityisanimportant characteristic

for cell viability.This study opens new perspectives to obtain

macrophagecellswithahighviability,avoidingsignificantlossof

viablecellswhichstilllimitsthecurrentscratchingprocedures

Fur-therstudieswillbeconductedinordertoevaluatetheimpactof thesubstitutiondegreeofAc-Stontheattachmentandactivityof macrophages

Acknowledgments

ThefinancialsupportfromNSERC(NaturalScienceand Engi-neering Research Council of Canada) Discovery Program is gratefullyacknowledged.ThanksareduetoDr.TienCanhLefor helpfuldiscussions

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