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Proteins,thebuildingblocksoflife,aresynthesizedbyalllivingformsaspart oftheirnaturalmetabolism.Someproteins,suchasenzymes,serveasbiocatal ystsandincreasetherateofmetabolicreactions,while

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ContentslistsavailableatScienceDirect BiotechnologyAdvances jou r n a lh o m e pag e :www.e l s ev i e r.co m/lo c a t e /b io te c h ad v

Researchreviewpaper

Productionofrecombinantproteinsbymicrobesandhigherorganisms

ArnoldL.Demaina,⁎ ,PreetiVaishnavb

a Resea

rchInstituteforScientistsEmeriti(R.I.S.E.),DrewUniversity,Madison,NJ07940,USA

b 206AkshardeepApts.,NearNewJainTemple,GIDC,Ankleshwar393002,Gujarat,India

a r t i c l ein f o

Articlehistory:

Received26September2008

Receivedinrevisedform14January2009

Accepted21January2009

Availableonline31January2009

Keywords:recombinan

tproteinsenzymes

bacteria

yeasts

filamentousfungiin

sectcellsmammalia

ncellstransgenicani

mals

transgenicplants

a b s t r a c t Largeproteinsareusuallyexpressedinaeukaryoticsystemwhilesmalleronesareexpressedinprokaryoticsystems.Fo rproteinsthatrequireglycosylation,mammaliancells,fungiorthebaculovirussystemischosen.Theleastexpensive,e asiestandquickestexpressionofproteinscanbecarriedoutinEscherichiacoli.However,thisbacteriumcannotexpress

verylargeproteins.Also,forS–Srichproteins,andproteinsthatrequirepost-translationalmodifications,E.coliisnotthesystemofchoice.ThetwomostutilizedyeastsareSaccharomycescerevisia eandPichiapastoris.Yeastscanproducehighyieldsofproteinsatlowcost,proteinslargerthan50kDcanbeproduced,signa lsequencescanberemoved,andglycosylationcanbecarriedout.Thebaculoviralsystemcancarryoutmorecomplexpos

t-translationalmodificationsofproteins.Themostpopularsystemforproducingrecombinantmammalianglycosylat edproteinsisthatofmammaliancells.Geneticallymodifiedanimalssecreterecombinantproteinsintheirmilk,bloodo rurine.Similarly,transgenicplantssuchasArabidopsisthalianaandotherscangeneratemanyrecombinantproteins.

©2009ElsevierInc.Allrightsreserved.

Contents

1.Introduction 297

2.Enzymeproduction 298

3.Systemsforproducingrecombinantproteins 298

3.1.Bacteria 299

3.1.1.E.coli 299

3.1.2.Bacillus 300

3.1.3.Otherbacteria 300

3.2.Yeasts 300

3.3.Filamentousfungi(molds) 302

3.4.Insectcells 302

3.5.Mammaliancells 302

3.6.Transgenicanimals 303

3.7.Transgenicplants 304

4.Conclusions 304

References 305

1.Introduction

⁎Correspondingauthor.DrewUniversity,R.I.S.E.,HS-330,Madison,NJ007940,USA.Tel.:

+19734083937;fax:+19734083504.

E-mailaddress: ademain@drew.edu (A.L.Demain).

Proteins,thebuildingblocksoflife,aresynthesizedbyalllivingformsaspart oftheirnaturalmetabolism.Someproteins,suchasenzymes,serveasbiocatal ystsandincreasetherateofmetabolicreactions,whileothersformthecytosk eleton.Proteinsplayasignificantroleincellsignaling,immuneresponses,cel ladhesion,

0734-9750/$–

seefrontmatter©2009ElsevierInc.Allrightsreserved.doi: 10.1016/

j.biotechadv.2009.01.008

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29 29

andthecellcycle.Theyarecommerciallyproducedinindustrieswiththeaidofg

eneticengineeringandproteinengineering.Nativeandrecombinantprotei

nsbenefitmajorsectorsofthebiopharmaceuticalindustry,theenzymeindu

stry,andtheagriculturalindustry.Productsoftheseindustriesinturnaugme

ntthefieldsofmedicine,diagnostics,food,nutrition,detergents,textiles,leat

her,paper,pulp,polymersandplastics.Thefirstproteinvaccineproducedwa

sthecow-poxvaccinebyJennerin1796.Themicrobialfermentationindustrywasborni

ntheearly1900swhenthefirstlarge-scaleanaerobicfermentationstomanufacturechemicalssuchasacetoneand

butanolbegan,followedbytheaerobicproductionofcitricacid.Penicillinwas

discoveredin

1927butitsdevelopmentdidnotoccuruntilthestartofthe1940s,priortothetimet

hatstreptomycinwasdiscovered.Thefirstproteinpharmaceuticalproduce

dwasinsulinbyBantingandBestin1922.Themodernbiotechnologyerabegan

in1971withtheestablishmentoftheCetusCorporationinCaliforniaabout1–

2yearsbeforethediscoveryofrecombinantDNAbyBerg,CohenandBoyerinC

alifornia.Thiswasfollowed5yearslaterbythestartofGenentech,andthenbyot

hercorporationssuchasAmgenandBiogen,etc

By2002,over155approvedpharmaceuticalsandvaccineshadbeendeve

lopedbybiopharmaceuticalcompanies.Today,morethan

200approvedpeptideandproteinpharmaceuticalsareontheFDAlist.Someof

therecombinantproteinpharmaceuticalsproducedarehumaninsulin,al

bumin,humangrowthhormone(HGH),FactorVIII,andmanymore.Biophar

maceuticalshavebeeninstrumentalinradi-callyimprovinghumanhealth(Swartz,1996):

(i)diabeticsnolongerhavetofearproducingantibodiestoanimalinsulin;

(ii)childrendeficientingrowthhormonenolongerhavetosufferfromdwarfis

morfeartheriskofcontractingKreutzfeld–Jacobsyndrome;(iii)chil-drenwhohavechronicgranulomatousdiseasecanleadanormallifebytakingg

ammainterferontherapy;and(iv)patientsundergoingcancerchemothera

pyorradiationtherapycanrecovermorequicklywithfewerinfectionswhe

ntheyusegranulocytecolony-stimulatingfactor(G-CSF).Manyotherexamplesoftheconquestofdiseasecouldbementioned

2.Enzymeproduction

Theenzymeindustryflourishedinthe1980sand1990swhenmicrobiale

nzymescameontothescene.Inthe1970s,mostoftheenzymesusedweretradit

ionallyderivedfromplantandanimalsources,whichresultedinalowlevelofa

vailability,highprices,andstuntedgrowthoftheenzymeindustry.Microbiale

nzymesprovedeconomicallyfavorablesincecultivationofmicrobeswasmu

chsimplerandfasterthanthatofplantsandanimalsandtheproducingorgani

smscouldbeeasilymanipulatedgeneticallytoproducedesiredqualitiesand

quantitiesofenzymes.Someofthemajorindustrialusesofenzymesinmanuf

acturinginclude(1)Escherichiacoliamidasetoproduce6-aminopenicillanicacid(6-APA)at40,000tons/year;

(2)StreptomycesxyloseisomerasetoisomerizeD-glucosetoD

-fructoseat100,000tons/

year;and(3)Pseudomonaschlorapisnitrilehydratasetoproduceacrylamide

fromacrylonitrileat30,000tons/

year(Jaegeretal.,2002).Amylasesareproducedatanannualrateof95,000ton

speryear.Thetotalmarketforindustrialenzymesreached$2billionin2000an

dhasrisento$2.5billiontoday.Theleadingenzymeisproteasewhichaccount

sfor57%ofthemarket.Othersincludeamylase,glucoamylase,xyloseisomer

ase,lactase,lipase,cellulase,pullulanaseandxylanase.Thefoodandfeedindu

striesarethelargestcustomersforindustrialenzymes.Overhalfoftheindustri

alenzymesaremadebyyeastsandmolds,withbacteriaproducingabout30

%.Animalsprovide8%andplants4%.Enzymesalsoplayakeyroleincatalyzingr

eactionswhichleadtothemicrobialformationofantibioticsandothersecond

arymetabolites

Overtheyears,highertitersofenzymeswereobtainedusing“brute

force”mutagenesisandrandomscreeningofmicroorganisms.Recom-binantDNAtechnologyactedasaboonfortheenzymeindustryinthe

followingways(Falch,1991):

(i)plantandanimalenzymescouldbemadebymicrobialfermentations,e.g.,c hymosin;

(ii)enzymesfromorganismsdifficulttogroworhandlegeneticallywerenow producedbyindustrialorganismssuchasspeciesofAspergillusandTrichoder ma,andKluyveromyceslactis,Saccharomycescerevisiae,Yarrowialipolyticaan dBacilluslicheniformis(e.g.,thermophiliclipasewasproducedbyAspergilluso

ryzaeandThermoanaerobactercyclodextringlycosyltrans-ferasebyBacillus);

(iii)enzymeproductivitywasincreasedbytheuseofmultiplegenecopies,stro ngpromotersandefficientsignalsequences;

(iv)productionofausefulenzymefromapathogenicortoxin-producingspeciescouldnowbedoneinasafehost;and(v)proteinengineering wasemployedtoimprovethestability,activityand/

orspecificityofanenzyme

Bythe1990s,manyenzymeswereproducedbyrecombinanttechniques In1993,over50%oftheindustrialenzymemarketwasprovidedbyrecombina ntprocesses(Hodgson,1994);saleswere

$140million(Stroh,1994 ).Plantphytase,producedinrecombinantAs- pergillusnigerwasusedasafeedfor50%ofallpigsinHolland.A1000-foldincreaseinphytaseproductionwasachievedinA.nigerbytheuseofrecom binanttechnology(VanHartingsveldtetal.,1993).Industriallipaseswerecl onedinHumicolaandindustriallyproducedbyA.oryzae.Theyareusedforlaund

rycleaning,inter-esterificationoflipidsandesterificationofglucosides,producingglycolipid

swhichhaveapplica-tionsasbiodegradablenon-ionicsurfactantsfordetergents,skincareproducts,contactlensesandasfood emulsifiers.MammalianchymosinwasclonedandproducedbyA.nigerorE.c oliandrecombinantchymosinwasapprovedintheUSA;itspricewashalfthato fnaturalcalfchymosin.Over60%oftheenzymesusedinthedetergent,foodan dstarchprocessingindustrieswererecombinantproductsasfarbackasthe mid-1990s(Cowan,1996)

Today,withtheaidofrecombinantDNAtechnologyandproteinengineeri

ng,enzymescanbetailor-madetosuittherequirementsoftheusersoroftheprocess.Itisnolongernecessa rytosettleforanenzyme'snaturalproperties.Enzymesofsuperiorqualityha

vebeenobtainedbyproteinengineering,specificallybysite- directedmuta-genesis.SinglechangesinaminoacidsequencesyieldedchangesinpHoptim

um,thermostability,feedbackinhibition,carbonsourceinhibi-tion,substratespecificity,Vmax,KmandKi.Anewandimportantmethodforim provingenzymeswasdirectedevolution(alsoknownasappliedmoleculare volutionordirectedmolecularevolution)(

Kuch-nerandArnold,1997;Arnold,1998;JohannesandZhao,2006).Unlikesitedirect edmutagenesis,thismethodofpoolingandrecombiningpartsofsimilargen esfromdifferentspeciesorstrainsyieldsremarkableimprovementsinenzy mesinaveryshortamountoftime.Theprocedureactuallymimicsnatureintha tmutation,selectionandrecombinationareusedtoevolvehighlyadaptedprot eins,butitismuchfasterthannature.Thetechniquecanbeusedtoimprovepro teinpharmaceuticals,smallmoleculepharmaceuticals,genetherapy,DNAv accines,recombinantproteinvaccines,viralvaccinesandtoevolveviruses.P roteinsfromdirectedevolutionworkwerealreadyonthemarketin2000(Tobi netal.,2000)

Manyenzymesareusedastherapeuticagentstotreatgastro- intestinalandrheumaticdiseases,thromboses,cysticfibrosis,meta-bolicdiseaseandcancer.Salesoftherapeuticenzymeswere

$2.3billionin1996whilein1998marketsfortherapeuticenzymeswereasfollo ws(Stroh,1999):Pulmozyme(DNase)forcysticfibrosis,acutemyocardialinf arctionandischemicstroke,$350million;Ceredase®and

Cerezyme®(

r-DNAversion)forGaucher'sdisease,

$387million.By2007,themarketforCerezyme®reached$1.1billion.Thether apeuticmarketisinadditiontotheindustrialenzymemarketdiscussedabo ve

3.Systemsforproducingrecombinantproteins Bymeansofgeneticengineering,desiredproteinsaremassivelygenerat edtomeetthecopiousdemandsofindustry.Hence,most

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binantproteinproductionisgettingthedesiredDNAcloned;thentheprotei

nisamplifiedinthechosenexpressionsystem.Thereisawidevarietyofprotein

expressionsystemsavailable.Proteinscanbeexpressedincellculturesofba

cteria,yeasts,molds,mammals,plantsorinsects,orviatransgenicplantsan

danimals.Proteinquality,functionality,productionspeedandyieldarethem

ostimportantfactorstoconsiderwhenchoosingtherightexpressionsyste

mforrecombinantproteinproduction

Asof2002,therewereabout140therapeuticproteinsapprovedinEurop

eandtheUSA(Walsh,2003

).Non-glycosylatedproteinsareusuallymadeinE.colioryeastsandtheyconstitute

40%ofthetherapeuticproteinmarket.N-glycosylatedproteinsareusuallymadeinmammaliancellswhichmimichum

anglycosylation.Chinesehamsterovary(CHO)cellsprovideabout50%ofthe

therapeuticproteinmarketbuttheprocessisveryexpensiveandtheglycopr

oteinsmadearenotexactlythehumantype,andinsomecases,theymustbem

odified.Yeasts,moldsandinsectcellsaregenerallyunabletoprovidemamm

alianglycosylation.However,thepopularmethylotrophicyeast,Pichiapast

oris,hasbeengeneticallyengineeredtoproduceahumantypeofglycosylatio

n(seebelow)

3.1.Bacteria

3.1.1.E.coli

E.coliisoneoftheearliestandmostwidelyusedhostsfortheproductionofh

eterologousproteins(Terpe,2006).Advantagesanddisadvantagesareshow

ninTable1.Theseincluderapidgrowth,rapidexpression,easeofcultureandhi

ghproductyields(Swartz,1996).Itisusedformassiveproductionofmanycom

mercializedproteins.Thissystemisexcellentforfunctionalexpressionofno

n-glycosylatedproteins.E.coligeneticsarefarbetterunderstoodthanthoseof

anyothermicroorganism.Recentprogressinthefundamentalunder-standingoftranscription,translation,andproteinfoldinginE.coli,together

withtheavailabilityofimprovedgenetictools,ismakingthisbacteriummor

evaluablethaneverfortheexpressionofcomplexeukaryoticproteins.Itsgen

omecanbequicklyandpreciselymodifiedwithease,promotorcontrolisnotdi

fficult,andplasmidcopynumbercanbereadilyaltered.Thissystemalsofeatu

resalterationofmetaboliccarbonflow,avoidanceofincorporationofamino

acidanalogs,formationofintracellulardisulfidebonds,andreproduciblepe

rfor-mancewithcomputercontrol.E.colicanaccumulaterecombinantproteins

upto80%ofitsdryweightandsurvivesavarietyofenvironmentalconditions

TheE.colisystemhassomedrawbacks,however,whichhavetobeoverco

meforefficientexpressionofproteins.Highcelldensitiesresultintoxicitydue

toacetateformation;however,thiscanbeavoidedbycontrollingthelevelofox

ygen.Proteinswhichareproducedasinclusionbodiesareofteninactive,inso

lubleandrequirerefolding.Inaddition,thereisaproblemproducingprotein

swithmanydisulfidebondsandrefoldingtheseproteinsisextremelydifficu

lt.TheE.colisystemproducesunmodifiedproteinswithoutglycosylationwh

ichisthereasonwhysomeproducedantibodiesfailtorecognizemamma-lianproteins(JenkinsandCurling,1994

).Surprisingly,thenon-glycosylatedhumantPAproducedinE.coliwasfullyactiveinvitro

Table1

CharacteristicsofE.coliexpressionsystems

AdvantagesDisadvantages

RapidexpressionProteinswithdisulfidebondsdifficulttoexpress

HighyieldsProduceunglycosylatedproteins

(Sarmientosetal.,1989 ).DespitethelackoftheusualtPAglycosyla-

tion,theproducthadafour-foldlongerhalf-lifeinplasmaandacorrespondinglongerclearancerateinanimals(Dartaretal ,1993).Theamountproducedwas5–10%oftotalE.coliprotein

ToimprovetheE.coliprocesssituation,thefollowingmeasureshavebeen taken:(i)useofdifferentpromoterstoregulateexpression;

(ii)useofdifferenthoststrains;(iii)co-expressionofchaperonesand/ orfoldases;(iv)loweringoftemperature;

(v)secretionofproteinsintotheperiplasmicspaceorintothemedium; (vi)reducingtherateofproteinsynthesis;(vii)changingthegrowthmedium; (viii)additionofafusionpartner;

(ix)expressionofafragmentoftheprotein;and(x)invitrodenaturationandref oldingoftheprotein(Swartz,2001;ChoiandLee,2004;Mergulhaoetal.,2005

;ShiloachandFass,2005;Maldonadoetal.,2007;Chou,2007;Wongetal.,200 8

HighcelldensityfermentationsofE.colihaveresultedindrycellcontentso f20to175g/

l(Lee,1996).Theacetateproductionandtoxicityproblemcanbesolvedbyfeed ingglucoseexponentially,andkeepingthespecificgrowthratebelowthatwh ichbringsonacetateproduction.Inthisway,yieldsashighas5.5g/Lofα-consensusinterferoninbrothwereattained(Fieshko,1989).Growthinalong

-termchemostat(219generationsunderthelowdilutionrateof0.05h−1)yiel dedanE.colimutantthathadanincreasedspecificgrowthrate,increasedbio massyields,shorterlagphase,lessacetateproductionandincreasedresistan cetostress(Weikertetal.,1997).Thisstrainproducedincreasedlevelsofsecre tedheterologousproteins(Weikertetal.,1998)

HeterologousproteinsproducedasinclusionbodiesinE.coliareinactive ,aggregatedandinsoluble,usuallypossessingnon-nativeintra-andinter-moleculardisulfidebondsandunusualfreecysteines(Fischeretal.,1993).To obtainactiveprotein,thesebodiesmustberemovedfromthecell,theproteins solubilizedbydenaturantswhichunfoldtheproteins,anddisulfidebondsm ustbeeliminatedusingreducingagents.Refoldingisaccomplishedbytherem ovalofthedenaturantandthereducingagent,followedbyrenaturationofthe protein.Renaturationprocessesusedinclude(i)airoxidation,

(ii)theglutathionereoxidationsystem,and(iii)themixeddisulfidesofprotei

n-S-sulfonateandprotein-S-glutathionesystem.Heterologousrecombinantproteinscanbemadeinbiol ogicallyactivesolubleformathighlevelswhentheirgenesarefusedtotheE.col ithioredoxingene(LaVallieetal.,1993 ).MurineIL-2,humanIL-3,murineIL- 4,murineIL-5,humanIL-6,humanM1P-lalpha,humanIL-11,humanM-CSL,murineL1F,murineSFandhumanBMP-2areproducedatlevelsof5– 20%oftotalproteinsasfusionsinE.colicytoplasm.Somefusionsretainthethi oredoxinpropertiesofbeingreleasedbyosmoticshockorfreeze/

thawmethods,andhighthermalstability.Thioredoxinissmall(11kD)andisno rmallyproducedat40%oftotalcellproteininsolubleform(Lunnetal.,1984).An otherusefulmethodofreducingtheformationofinclusionbodiescontainin gheterologousproteinsistolowerthetemperatureofgrowthfrom 37°Cto30°C(Schein,1989)

Higheryieldsarenormallyproducedinthecytoplasmthanintheperiplas micspace.Cytoplasmicproteinscanbeexportedtosimplifypurificationandf acilitatecorrectfolding.Thismustbedonewithproteinscontainingdisulfide bondssincethecytoplasmistooreducinganenvironment.Tosecretethese proteinsintotheperiplasm,afusionismadewithaleaderpeptideattheN-terminus.Togettheproteinsoutoftheperiplasmandintothemedium,osmotic shockorcellwallpermeabilizationisused.Toincreaseproduction,apromoter system(lac,tac,trc)isused.Promotersystemsmustbestrongandtightlyregul

atedsothattheyhavealow-basallevelofexpression,easilytransferabletootherE.colistrains,andhaveasi mpleandinexpensiveinductiontechnique,independentofmediaingredie nts

Easeofcultureandgenomemo

difications Proteinsproducedwithendotoxins

SecretionofrecombinantproteinsbyE.coliintotheperiplasmorinto themediumhasmanyadvantagesoverintracellularproductionas

InexpensiveAcetateformationresultingincelltoxicity inclusionbodies.Ithelpsdownstreamprocessing,foldingandinvivo

Massproductionfastandcosteffe

ctive

Proteinsproducedasinclusionbodies,areinactive;

requirerefolding. stability,andallowstheproductionofsoluble,activeproteinsatareducedpr

ocessingcost(Mergulhaoetal.,2005).Highlevelexcretion

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30 30

Table2

AdvantagesofBacillusexpressionsystems

Strongsecretionwithnoinvolvementofintracellularinclusionbodies

Easeofmanipulation

Geneticallywellcharacterizedsystems

Highlydevelopedtransformationandgenereplacementtechnologies.Supe

riorgrowthcharacteristics

Metabolicallyrobust

Generallyrecognizedassafe(GRASstatus)byUSFDAEfficie

ntandcosteffectiverecovery

hasbeenobtainedwiththefollowingheterologousproteins:PhoA(alkalin

ephosphatase)at5.2g/

Lintotheperiplasm;LFT(levanfructotransferase)at4g/

Lintothemedium;hGCSF(humangranulocytecolony-stimulatoryfactor)at3.2g/

Lintotheperiplasm;cellulosebindingdomainat2.8g/

Lintotheperiplasm;IGF-1(insulin-likegrowthfactor)at2.5g/

Lintotheperiplasm;choleratoxinBat1g/

Lintothemedium(Mergulhaoetal.,2005).Asearlyas1993,recombinantproc

essesinE.coliwereresponsibleforalmost$5billionworthofproducts,i.e.,ins

ulin,humangrowthhormone,α,β,γ-interferonsandG-CSF(Swartz,1996)

3.1.2.Bacillus

OtherusefulbacterialsystemsarethoseoftheGram-positivebacilli.Thesearemainlypreferredforhomologousexpressionofenzy

messuchasproteases(fordetergents)andamylases(forstarchandbaking).So

meadvantagesofusingBacillussystemsareshowninTable2.Someoftheseadv

antagesareonlypresentinindustrialstrainswhichareoftenunavailabletoaca

demicresearchers.Inaddition,thegenomesofBacillussubtilisandB.lichenifo

rmishavebeensequenced,andthereisnoproductionofharmfulexotoxinsore

ndotoxins.Thesecretionofthedesiredproteinsintothefermentationmediu

mresultsineasydownstreamprocessing,eliminatingtheneedforcelldisrupt

ionorchemicalprocessingtechniques.Thismakesrecoveryrelativelyeffici

entandcost-effective.ThespeciesgenerallyusedforexpressionareBacillusmegaterium,

B.subtilis,B.licheniformisandBacillusbrevis.Theydonothavelipopolysacchar

ide-containingoutermembranesasdoGram-negativebacteria.IndustrialstrainsofB.subtilisarehighsecretorsandhoststr

ainsusedforsuccessfulexpressionofrecombinantproteinsareoftendeleted

forgenesamyE,aprE,nprE,spoIIAC,srfCandtransformedvianaturalcompe-tence.Bacillusproteinyieldsareashighas3g/L

ThereisaproblemwithB.subtilisbecauseofitsproductionofmanyprotea

seswhichsometimesdestroytherecombinantproteins.Theyincludeseven

knownproteases(Heetal.,1991),fiveofwhichareextracellular:

(i)Subtilisin(aprEgene):majoralkalineserineprotease

(ii)Neutralprotease(nprE):majormetalloprotease,containsZn

(iii)Minorserineprotease(epr);inhibitedbyphenylmethanesulfo-nylfluoride(PMSF)andethylenediaminetetraaceticacid

(EDTA)

(iv)BacillopeptidaseF(bpf):anotherminorserineprotease/ester-ase;inhibitedbyPMSF

(v)Minormetalloesterase(mpe)

(vi)ISP-I(isp-I):majorintracellularserineprotease,requiresCa

(vii)ISP-II(isp-II):minorintracellularserineprotease

Thefirsttwoenzymesaccountfor96–

98%oftheextracellularproteaseactivity.Otherresearchgroupshavereporte

dsixtoeightextracellularproteases.Wuetal

(1991)removedsixandonly0.32%activityremained.Growthinthepresence

of2mMPMSFeliminatedalltheproteaseactivity.AB.subtilisstrainhasbeend

evelopedforgeneticengineeringwhichisdeficientineightextracellularpro

teases(Murashimaetal.,2002).Carehastobetakenwithregardtoexcessivegr

owthratesandaeration.Productionofextracellularhumanalpha

interferonbyB.subtilisisrepressedbyhighgrowthrateandbyexcessoxygen( MeyerandFiechter,1985)

Anexoprotease-deficientB.licheniformishoststrainhasbeenspecificallytailoredforheterolo

gousgeneexpression.Itisaspor-ogenousandgiveshighextracellularexpressionlevelswithminimallossofpr oductduetoproteolyticcleavagesubsequenttosecretion.Toobtainamorege neticallystablesystemaftertransformationandtoincreaseproductionlevel

s,theα-amylasegenehasalsobeenremoved.Acomparisonofhostorganismswasma

deforproductionofinterleukin-3(vanLeenetal.,1991)amongE.coli,B.licheniformis,S.cerevisiae,K.lactisandC1 27mammaliancells.ThebestsystemwasreportedtobeB.licheniformis B.brevisisalsousedtoexpressheterologousgenesduetoitsmuchlowerpro teaseactivityandproductionofaproteinaseinhibitor(UdakaandYamagata,1

994).HumanepidermalgrowthfactorwasproducedinB.brevisatalevelof3g/ L(Ebisuetal.,1992)

HeterologousproteinssuccessfullyexpressedinBacillussystemsinclud

einterleukin-3EGFandesterasefromPseudomonas.Homolo-gousproteinsincludeBacillusstearothermophilusxylanase,naproxenester ase,amylasesandvariousproteases

3.1.3.Otherbacteria AnimprovedGram-negativehostforrecombinantproteinproduc-tionhasbeendevelopedusingRalstoniaeutropha(Barnardetal.,

2004.)ThesystemappearssuperiortoE.coliwithrespecttoinclusionbodyfor

mation.Organophosphohydrolase,aproteinpronetoinclu-sionbodyformationwithaproductionoflessthan100mg/

LinE.coli,wasproducedat10g/

LinR.eutropha.ThePfenexsystemusingPseudomonasfluorescenshasyielded

4g/LoftrimericTNF-alpha(SquiresandLucy,2008).Staphylococcuscarnosuscanproduce2g/ LofsecretedmammalianproteinwhereasthelevelmadebyStreptomyceslivi dansis0.2g/L(Hanssonetal.,2002)

3.2.Yeasts Yeasts,thesingle-celledeukaryoticfungalorganisms,areoftenusedtoproducerecombinantpr oteinsthatarenotproducedwellinE.colibecauseofproblemsdealingwithfo ldingortheneedforglycosylation.Themajoradvantagesofyeastexpressions ystemsarelistedinTable3.Theyeaststrainsaregeneticallywellcharacterized andareknowntoperformmanyposttranslationalmodifications.Theyareeas ierandlessexpensivetoworkwiththaninsectormammaliancells,andareeasily adaptedtofermentationprocesses.ThetwomostutilizedyeaststrainsareS.ce revisiaeandthemethylotrophicyeastP.pastoris.Variousyeastspecieshavepro ventobeextremelyusefulforexpressionandanalysisofrecombinanteukary oticproteins.Forexample,A.nigerglucoseoxidasecanbeproducedbyS.cerev isiaeat

9g/L

S.cerevisiaeofferscertainadvantagesoverbacteriaasacloninghost(Gellis onetal.,1992).(i)Ithasalonghistoryofuseinindustrialfermentation

(ii)Itcansecreteheterologousproteinsintothe

Table3 Advantagesofyeastexpressionsystems Highyield

Stableproductionstrains Durability

Costeffective Highdensitygrowth Highproductivity Suitabilityforproductionofisotopically-labeledprotein RapidgrowthinchemicallydefinedmediaProductp rocessingsimilartomammaliancellsCanhandleS–

Srichproteins Canassistproteinfolding

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ructuralgenes

(iii)Itcarriesoutglycosylationofproteins.However,glycosylationbyS.cerev

isiaeisoftenunacceptableformammalianproteinsbecausetheO-linkedoligosaccharidescontainonlymannosewhereashighereukaryotic

proteinshavesialylatedO-linkedchains.Furthermore,theyeastover-

glycosylatesN-

linkedsitesleadingtoreductioninbothactivityandreceptor-binding,andmaycauseimmunologicalproblems.Productsonthemarketwh

icharemadeinS.cerevisiaeareinsulin,hepatitisBsurfaceantigen,urateoxid

ase,glucagons,granulocytemacrophagecolonystimulatingfactor(GM-CSF),hirudin,andplatelet-derivedgrowthfactor

Almostallexcretedeukaryoticpolypeptidesareglycosylated.Glycosyl

ationisspecies-,tissue-andcell-type-specific(Parekh,1989).Insomecases,anormallyglycosylatedproteinisactiv

ewithoutthecarbohydratemoietyandcanbemadeinbacteria.Thisisthecase

withγ-interferon(Rinderknechtetal.,1984).Incaseswhereglycosylationisnecess

aryforstabilityorproperfolding(e.g.,erythropoietinandhumanchorionicgo

nadotropin),thiscanoftenbeprovidedbyrecombinantyeast,mold,insector

mammaliancells.MammaliansecretedproteinsareglycosylatedwithD

-mannosesugarscovalentlyboundtoaspar-agine-linkedN-acetyl-D

-glucosaminemolecules.Fungalenzymeswhichareexcretedoftenshowthes

ametypeofglycosylation(ElbeinandMolyneux,1985),althoughadditional

carbohydrateslinkedtotheoxygenofserineorthreoninesometimesarepre

sentinfungalproteins(Nunbergetal.,1984)

Theglycosylationofaproteincanbedifferentdependingonfactorssuchas

themediuminwhichthecellsaregrown.Theglycosylationinfluencesthereac

tionkinetics(iftheproteinisanenzyme),solubility,serumhalf-life,thermalstability,invivoactivity,immunogenicityandreceptorbinding

.Withregardtopeptides,galactosylatedenkephalinsare1000–

10,000timesmoreactivethanthepeptidealone(Warren,

1990).Thatglycosylationincreasesthestabilityofproteins,isshownby

cloninggenesencodingbacterialnon-glycosylatedproteinsinyeast.Theyeastversionswereglycosylatedandmor

estable(Dixon,1991).Glycosylationalsoaffectspharmacokinetics(residen

cetimeinvivo)

(JenkinsandCurling,1994).Examplesofstabilityenhancementaretheprotec

tionagainstproteolyticattackbyterminalsialicacidonerythropoietin(EPO

)(Goldwasseretal.,1974),TissuePlasminogenActivator(TPA)

(WittwerandHoward,1990)andinterferons(Cantelletal.,1992).Withregard

toactivity,humanEPOis1000-foldmoreactiveinvivothanitsdesialylatedformbuttheybothhavesimilarinvi

troactivities(Yamaguchietal.,1991

).Glycosylationoccursthrough(i)anN-

glycosidicbondtotheR-groupofanasparagineresidueinasequenceAsn-X-

Ser/Thr;or(ii)anO-glycosidicbondtotheR-groupofserine,threonine,hydroxprolineorhydroxylysine.However,thes

eaminoacidsmayonlybepartiallyglycosylatedorunglycosylatedleadingto

theproblemofheterogeneity.Inthefuture,clonedglycosyltransferaseswill

beusedtoensurehomogeneity(“glycosylationengineering”)

Methylotrophicyeastshavebecomeveryattractiveashostsforthe

industrialproductionofrecombinantproteinssincethepromoterscontrolli

ngtheexpressionofthesegenesareamongthestrongestandmoststrictlyreg

ulatedyeastpromoters.Thecellsthemselvescanbegrownrapidlytohighden

sities,andthelevelofproductexpressioncanberegulatedbysimplemanipula

tionofthemedium.Methylo-trophicyeastscanbegrowntoadensityashighas130g/

L(Gellisonetal.,1992).Thefourknowngeneraofmethylotrophicyeast(Han

senula,Pichia,Candida,andTorulopsis)shareacommonmetabolicpathwayt

hatenablesthemtousemethanolasasolecarbonsource.Inatranscriptionall

yregulatedresponsetomethanolinduction,severaloftheenzymesarerapid

lysynthesizedathighlevels

ThemajoradvantageofPichiaoverE.coliisthattheformeriscapableofpro

ducingdisulfidebondsandglycosylationofproteins.Thismeansthatincases

wheredisulfidesarenecessary,E.colimightproduceamisfoldedprotein,w

hichisusuallyinactiveorinsoluble.Comparedtootherexpressionsystemss

uchasS2-cellsfromDrosophilamelanogasterorChineseHamsterOvary(CH0)cells,Pichi

ausuallygivesmuchbetter

yields.Celllinesfrommulticellularorganismsusuallyrequirecomplex(rich) media,therebyincreasingthecostofproteinproductionprocess.Additiona lly,sincePichiacangrowinmediacontainingonlyonecarbonsourceandonenitr ogensource,itissuitableforisotopiclabellingapplicationsine.g.proteinNM R.AnadvantageofthemethylotrophP.pastoris,ascomparedtootheryeastsi nmakingrecombinantproteins,isitsgreatabilitytosecreteproteins.Succes shasbeenachievedingeneticallyengineeringtheP.pastorissecretorypathw

aysothathumantypeN-glycosylatedproteinsareproduced(Choietal.,2003).Amongtheadvantageso fmethylotrophicyeastsoverS.cerevisiaeasacloninghostarethefollowing: (i)higherproteinproductivity;(ii)avoidanceofhyperglycosylation; (iii)growthinreasonablystrongmethanolsolutionsthatwouldkillmostothe rmicroorganisms,

(iv)asystemthatischeaptosetupandmaintain,and(v)integrationofmulticop iesofforeignDNAintochromosomalDNAyieldingstabletransformants(G ellisonetal.,

1992)

GlycosylationislessextensiveinP.pastoristhaninS.cerevisiae(Daleetal.,1

999 )duetoshorterchainlengthsofN-linkedhigh-mannoseoligosaccharides,usuallyupto20residuescomparedto50–

150residuesinS.cerevisiae.P.pastorisalsolacksα-1,3- linkedmannosyltransferasewhichproducesα-1,3-linkedmannosylterminallinkagesinS.cerevisiaeandcausesahighlyantigeni cresponseinpatients.Hirudin,athrombininhibitorfromthemedicinalleech ,Hirudomedicinalisisnowmadebyrecombinantyeast(Sohnetal.,2001).Prod uctivitiesofhirudinindifferentsystemsareshowninTable4

P.pastorisproduceshighlevelsofmammalianrecombinantproteinsinth eextracellularmedium.Aninsulinprecursorwasproducedat1.5g/ L(Wangetal.,2001).Otherreportsinclude4g/

Lofintracellularinterleukin2as30%ofprotein,4g/

Lofsecretedhumanserumalbumin(Creggetal.,1993),6g/

Loftumornecrosisfactor(Daleetal.,1999)andotherheterologousproteins(M acauly-Patricketal.,

2005),and10g/

Loftumornecrosisfactor(Sreekrishanaetal.,1989).Productionofserumalb umininS.cerevisiaeamountedto0.15g/LwhereasinP.pastoris,thetiterwas10g/ L(Nevalainenetal.,2005).GelatinhasbeenproducedinP.pastoris,atover14g/ L(Wertenetal.,

1999).P.pastorisyielded300mg/l/

dayofrecombinanthumanchitinase(Goodricketal.,2001).Intracellulartet anustoxinfragmentCwasproducedas27%ofproteinwithatiterof12g/ L(Clareetal.,

1991).ClaimshavebeenmadethatP.pastoriscanmake20–30g/lof recombinantproteins(Morrow,2007)

Therearehowever,somedisadvantagesofusingPichiaasahostforheterolo gousexpression.Anumberofproteinsrequirechaperoninsforproperfoldin g.Pichiaisunabletoproducesuchproteins.AgroupledbyGerngrossmanage dtocreateastrainthatproducesEPOinitsnormalhumanglycosylationform( Gerngross,2004;Hamiltonetal.,

2006).Thiswasachievedbyexchangingtheenzymesresponsiblefortheyeastt ypeofglycosylation,withthemammalianhomologs.Thus,thealteredglycos ylationpatternallowedtheproteintobefullyfunctionalinhumansandsincet hen,thishumanglycosylationofrecombinantproteinsmadeintheengineer edP.pastorishasbeenshownwithotherhumanproteins

HeterologousgeneexpressioninanothermethylotrophHansenulapoly morphayielded1g/LofintracellularhepatitisBS-antigen(50genecopies/ cell),1.4g/Lofsecretedglucoamylase(4copies/cell),and

Table4 Comparisonofproductivitiesofhirudinbyrecombinanthosts Recombinanthostsmg/LBHKcells0.05

Insectcells0.40 Streptomyceslividans0.25–0.5 Escherichiacoli200–300 Saccharomycescerevisiae40–500 Hansenulapolymorpha1500 Pichiapastoris1500

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byK.lactis

3.3.Filamentousfungi(molds)

FilamentousfungisuchasA.nigerareattractivehostsforrecombinantD

NAtechnologybecauseoftheirabilitytosecretehighlevelsofbioactiveprote

inswithpost-translationalprocessingsuchasglycosylation.A.nigerexcretes25g/

Lofglucoamylase(Wardetal.,

2006

).Foreigngenescanbeincorporatedviaplasmidsintochromo-somesofthefilamentousfungiwheretheyintegratestablyintothechromoso

meastandemrepeatsprovidingsuperiorlong-termgeneticstability.Asmanyas100copiesofagenehavebeenobserved.Tri

chodermareeseihasbeenshowntoglycosylateinamannersimilartothatin

mammaliancells(Salovourietal.,1987)

Thetiterofagenetically-engineeredbovinechymosin-producingstrainofAspergillusawamoriwasimproved500%byconventiona

lmutagenesisandscreening(LamsaandBloebaum,1990).Itwasthenincrease

dfrom250mg/Lto1.1g/Lbynitrosoguanidinemutagenesisandselectionfor2-deoxyglucoseresistance(Dunn-Colemanetal.,

1991,1993).Transformantscontained5–10integratedcopiesofthe

chymosingene.ProductionofhumanlactoferrinbyA.awamoriviarDNAtec

hnologyandclassicalstrainimprovementamountedto2g/

Lofextracellularprotein(Wardetal.,1995).A.nigerglucoamylasewasmadeb

yA.awamoriat4.6g/

L.Humanizedimmunoglobulinfulllengthantibodieswereproducedandse

cretedbyA.niger.Themono-clonalantibodyTrastazumabwassecretedat0.9g/L(Wardetal.,

2004).RecombinantA.oryzaecanproduce2g/Lofhumanlactoferrin

(Wardetal.,1995)and3.3g/LofMucorrennin(Christensenetal.,

1988).FusariumalkalineproteaseisproducedbyAcremoniumchrysogenu

mat4g/L.Recombinantenzymeproductionhasreached

35g/

LinT.reesei(DurandandClanet,1988).ThefungusChrysosporiumlucknow

ensehasbeengeneticallyconvertedintoanon-

filamentous,lessviscous,lowprotease-producingstrainthatiscapableofproducingveryhighyieldsofheterologous

proteins(Verdoesetal.,2007).DyadicInternationalInc.,thecompanyrespo

nsibleforthedevelopmentoftheC.lucknowensesystem,claimsproteinprod

uctionlevelsofupto100g/Lofprotein

Despitetheabovesuccesses,secretedyieldsofsomeheterologousprotei

nshavebeencomparativelylowinsomecases.Thestrategiesforyieldimprov

ementhaveincludeduseofstronghomologouspromoters,increasedgeneco

pynumber,genefusionswithageneencodinganaturallywell-

secretedprotein,protease-deficienthoststrains,andscreeningforhightitersfollowingrandommuta

genesis.Suchapproacheshavebeeneffectivewithsometargetheterologous

proteinsbutnotwithothers.Hence,althoughtherehasbeenanimprovemen

tintheproductionoffungalproteinsbyrecombinantDNAmethods,thereare

usuallytranscriptionlimitations(Verdoesetal.,1995).Althoughanincrease

ingenecopiesuptoaboutfiveusuallyresultsinanequivalentincreaseinprotei

nproduction,highernumbersofgenecopiesdonotgiveequivalentlyhighlevel

sofprotein.SincethelevelofmRNAcorrelateswiththelevelofproteinproduc

ed,transcriptionisthemainproblem.Studiesonoverproductionofglucoa

mylaseinA.nigerindicatetheproblemintranscriptiontobedueto(i)thesiteofi

ntegrationoftheintroducedgenecopiesand(ii)theavailableamountoftrans-acting

Table5

Advantagesofbaculoviralinfectedinsectcellexpressionsystem

Posttranslationalmodifications

ProperproteinfoldingH

ighexpressionlevelsEas

yscaleup

Safety

Flexibilityofproteinsize

Efficientcleavageofsignalpeptides

Multiplegenesexpressedsimultaneously

regulatoryproteins.Also,heterologousproteinproductionbyfilamen-tousfungiissometimesseverelyhamperedbyfungalproteases.Aspergillusni dulanscontainsabout80proteasegenes(Machida,2002)

3.4.Insectcells Insectcells(Table5 )areabletocarryoutmorecomplexpost-translationalmodificationsthancanbeaccomplishedwithfungi.Theyalsoha vethebestmachineryforthefoldingofmammalianproteinsandaretherefore quitesuitableformakingsolubleproteinofmammalianorigin(Agathos,199

1).Themostcommonlyusedvectorsystemforrecombinantproteinexpressi onininsectsisthebaculovirus.Themostwidelyusedbaculovirusisthenuclea rpolyhedrosisvirus(Autographacalifornica)whichcontainscirculardouble

-strandedDNA,isnaturallypathogenicforlepidopterancells,andcanbegrow neasilyinvitro.Theusualhostisthefallarmyworm(Spodopterafrugiperda)ins uspensionculture.Alarvalculturecanbeusedwhichismuchcheaperthanam ammaliancellculture.Recombinantinsectcellcultureshaveyieldedover200 proteinsencodedbygenesfromviruses,bacteria,fungi,plantsandanimals(K night,1991

).Thebaculovirus-assistedinsectcellexpressionoffersmanyadvantages,asfollows

(i)Eukaryoticpost- translationalmodificationswithoutcomplication,includingphosphor-

ylation,N-andO-glycosylation,correctsignalpeptidecleavage,properproteolyticprocessin

g,acylation,palmitylation,myristylation,amida-tion,carboxymethylation,andprenylation(LuckowandSummers,1988;Mil ler,1988).(ii)ProperproteinfoldingandS–

Sbondformation,unlikethereducingenvironmentofE.colicytoplasm (iii)Highexpressionlevels.Theviruscontainsageneencodingtheproteinpoly hedrinwhichismadeatveryhighlevelsnormallyandisnotnecessaryforvirusr eplication.Thegenetobeclonedisplacedunderthestrongcontroloftheviralp olyhedrinpromoter,allowingexpressionofheterologousproteinofupto30

%ofcellprotein.Productionofrecombinantproteinsinthebaculovirusexpr essionvectorsystemininsectcellsreached

600mg/

Lin1988(MaiorellaandHarano,1988).Recentinformationindicatesthattheb aculovirusinsectcellsystemcanproduce11g/

Lofrecombinantprotein(Morrow,2007 ).(iv)Easyscaleupwithhigh-densitysuspensionculture

(v)Safety;expressionvectorsarepreparedfromthebaculoviruswhichcanatta ckinvertebratesbutnotvertebratesorplants,thusinsuringsafety

(vi)Lackoflimitonproteinsize.(vii)Efficientcleavageofsignalpeptides (viii)Simultaneousexpressionofmultiplegenes(WilkinsonandCox,1998) Insectcellsystemshowever,dohavesomeshortcomings,someofwhichc

anbeovercome.(i)Particularpatternsofpost-translationalprocessingandexpressionmustbeempiricallydeterminedfor eachconstruct

(ii)Differencesinproteinsexpressedbymammalianandbaculovirus-infectedinsectcells.Forexample,inefficientsecretionfrominsectcellsmaybe circumventedbytheadditionofinsectsecretionsignals(e.g.,honeybeemelit tinsequence)

(iii)Improperlyfoldedproteinsandproteinsthatoccurasintracellularaggre gatesaresometimesformed,possiblyduetoexpressionlateintheinfectioncy cle.Insuchcases,harvestingcellsatearliertimesafterinfectionmayhelp (iv)Lowlevelsofexpression.Thiscanoftenbeincreasedwithoptimizationoft imeofexpressionandmultiplicityofinfection

(v)Incorrectglycosylationhasbeenaproblemwithinsectcellsashosts(Bisbe e,1993).Thecompleteanalysisofcarbohydratestructureshasbeenreported

foralimitednumberofglycoproteins.PotentialN-linkedglycosylationsitesareofteneitherfullyglycosylatedornotglycosylate datall,asopposedtoexpressionofvariousglycoformsthatmayoccurinmamm

aliancells.Species-specificortissue-specificmodificationsareunlikelytooccur

3.5.Mammaliancells Mammalianexpressionsystemsareoftenusedforproductionofproteinsr

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equiringmammalianpost-translationalmodifications.Theuseofmammaliancellculture,chieflyimmo rtalizedChinesehamster

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eplasminogenactivator(tPA)productionintheearlydaysofthebiopharmace

uticaleffort,i.e.,inthe1980s(Swartz,1996).Theseglycosylatedproteinscould

notbeproducedinE.coliatthattime.CHOcellsconstitutethepreferredsystem

forproducingmonoclonalanti-bodiesorrecombinantproteins.Othercelltypesinclude(i)variousmousem

yelomassuchasNS0murinemyelomacells(AndersenandKrummen,2002),

(ii)SF-9,aninsectcellline,

(iii)babyhamsterkidney(BHK)cellsforproductionofcattlefoot-and-mouthdiseasevaccine,

(iv)greenmonkeykidneycellsforpoliovaccine(Wrotnowski,1998)and(v)h

umancelllinessuchashumanembryonickidney(HEK)cells.NSOisanonsecr

etingsubcloneoftheNS-1mousemelanomacellline.In1997,salesofbiotherapeuticsproducedbycell

culturewere

$3.25billionwhereasE.colibasedbiotherapeuticsamountedto

$2.85billion(Langer,1999).By2006,productionoftherapeuticproteinsbyma

mmaliansystemsreached$20billion(Griffinetal.,

2007)

Mammaliancellculturesareparticularlyusefulbecausetheproteinsareo

ftenmadeinaproperlyfoldedandglycosylatedform,thuseliminatingthenee

dtorenaturethem.Eukaryoticcellsarealsousefulforadditionoffattyacidchain

sandforphosphorylatingtyrosine,threonineandserinehydroxylgroups(Qi

u,1998).Mamma-liancellshavehighproductivityof20–60pg/cell/

day.HumantPAwasproducedinCHOcellsat34mg/

Lwithanoverallyieldof47%.AlthoughproductioninE.coliwasatamuchhigh

erlevel(460mg/

L),recoverywasonly2.8%duetoproductionasinclusionbodiesandlowrenat

urationyields(Dartaretal.,1993).Genesfortheglycosylatedfertilityhormone

s,humanchorionicgonadotropin,andhumanluteinizinghormonehavebe

enclonedandexpressedinmammaliancells.Recombinantproteinproducti

oninmammaliancellsrosefrom

50mg/Lin1986to4.7g/

Lin2004mainlyduetomediaimprovementsyieldingincreasedgrowth(Aldr

idge,2006).Atiterof2.5–3g/

Lproteinin14dayCHOfedbatchshakeflaskculturewasachievedusingFe2(Se

O3)3asioncarrier(Zhangetal.,2006).Anumberofmammalianprocessesarepr

oducing3–5g/Land,insomecases,proteintitershave

reached10g/

Linindustry(Ryll,2008).Arathernewsystemisthatofahumancelllineknown

asPER.C6ofCrucellHollandBV,which,incooperationwithDSMBiologics,w

asreportedtoproduce15g/

L(CocoMartinandHarmsen,2008)andthenlater,26g/

Lofamonoclonalantibody(Jarvis,2008)

Manyantibodieswereproducedinmammaliancellcultureatlevelsof0.7

–1.4g/

L.However,highervalueshavebeenreportedrecently.Forexample,monoc

lonalantibodyproductioninNSOanimalcellsreachedover2.5g/linfed-batchprocesses(ZhangandRobinson,

2005

).Animal-free,protein-freeandevenchemically-definedmediawithgoodsupportofproductionhavebeendeveloped.ThePfi

zerorganizationreportedmonoclonalantibodytitersof2.5–3.0g/Linnon-optimizedshakeflaskexperiments(Yu,2006)

Mammaliansystemsdohavesomedrawbacksasfollows

(i)Poorsecretion.Productionofsecretedforeignproteinsbymammaliancel

lsinthe1990samountedto1to10mg/Lwithspecificproductivitiesof

0.1to1pg/cell/

day(WurmandBernard,1999).Theprocessdurationwas5to10days.Althoug

hhighertitershavebeenreached,acceptablelevelswere10–20mg/L

(ii)Mammalianprocessesareexpensive.Thesellingprices(pergram)ofreco

mbinantproteinswere$375forhumaninsulin,$23,000fortPA,

$35,000forhumangrowthhormone,

$384,000forGM-CSF,$450,000forG-CSF,and$840,000forEPO.Allexcepthumaninsulinweremadeinmammali

ancellcultures(Bisbee,

1993).Themanufacturingofmammaliancellbiopharmaceuticalsinafullyva

lidatedplantrequires2to4milliondollarsperyearincostsofmaterialsespecia

llyformedia,15to20milliondollarsperyearinmanufacturingcosts(includin

goverhead,materialandlabor)and40to60milliondollarstoconstructafacility

of25,000ft2and

tovalidateit.AddedontothisisahugecostforgettingFDAapprov al,includingproofofconsistentperformance,productionofabioactiveprod uct,andlackofcontaminationbyvirusesandDNA.Clinicaltrialsand

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100milliondollars(Bisbee,1993)

(iii)Mammaliancellprocessesalsohaveapotentialforproductcontaminati onbyviruses(Bisbee,1993)

3.6.Transgenicanimals

Transgenicanimalsarebeingusedforproductionofrecombinantprotein sinmilk,eggwhite,blood,urine,seminalplasmaandsilkwormcocoons.Thusf ar,milkandurineseemtobebest.Foreignproteinscanbeproducedinthemamm aryglandsoftransgenicanimals(Bremetal.,1993).Transgenicanimalssucha sgoats,mice,cows,pigs,rabbit,andsheeparebeingdevelopedasproductionsy stems;someaquaticanimalsarealsobeingutilized.Transgenicmiceproduce

tPAandsheepß-lactoglobulinandtransgenicsheepproducehumanFactorIXintheirmilk.Tr ansgenicsheephavebeendevelopedwhichproducemilkcontaining35g/

Lofhumanα-1-antitrypsin,aserumglycoproteinapprovedintheU.S.foremphysema(Wrig htetal.,1991).tPAhasbeenmadeinmilkoftransgenicgoatsatalevelof3g/ L(Glanz,1992).RecombinanthumanproteinC(ananticoagulant)isproduc edinthemilkoftransgenicpigsattherateof

1g/L/

h(Velanderetal.,1992).Cowsproduce30Lofmilkperdaycontainingproteinat 35g/L;thusthetotalproteinproducedperdayis

1kg.Evenifarecombinantproteinwasonlymadeat2g/

L,theannualproductionpercowwouldbe10kg

Theamountsofmilkproducedbyanimals(L/

year)are8000percow,1000pergoat,300persheepand8perrabbit(Rudolph,19

97 ).Productiontiterswere14g/Lofanti-thrombinIIIingoatmilk,35g/Lofα-

1-antitrypsininsheepmilk,and8g/Lofα-glucosidaseinrabbitmilk;allgeneswerefromhumans.Transgenicexpressi onofforeignmilkproteinshasyieldedtitersashighas23g/

Lalthoughtheusualfigureisabout1g/L.Transgenicsheepproduce5g/ Lofrecombinantfibrinogenforuseasatissuesealantand0.4g/

LrecombinantactivatedproteinC,ananticoagulantusedtotreatdeep-veinthrombosis(Dutton,1996).Humanhemoglobinisproducedinpigsat40

g/L.Transgenicexpressionofforeignnon-milkproteinsisusuallymuchlessthanthatofmilkproteins.However,anexc

eptionisthatofhumanα-1-antitrypsininsheepasmentionedabove(Wrightetal.,1991).Inmostcases,the proteinisasactiveasthenativeprotein.Titersofhumangrowthhormoneinmi lkofmiceare4g/Landthatofanti-thrombinIIIis2g/

L.Productioninmilkismorecost-effectivethanthatinmammaliancellculture.Dairyanimalsproduce1to14g /

Lofheterologousproteininmilkeverydayforthe305daylactationcycleeachy ear.TransgenicgoatsproducetPAwithaglycosylationpatterndifferentfrom thatproducedincellcultureandwithalongerhalflifethannativetPA.Transg enicanimalproductshavebeentestedinhumanclinicaltrialsandnoadverser eactionsorsafetyconcernswerereported(McKownandTeutonico,1999) Humangrowthhormonehasbeenproducedintheurineoftransgenicmic e(Kerretal.,1998)butonlyat0.1–0.5mg/

L.Oneadvantageofusingthebladderasabioreactorinsteadofthemammary glandisthatanimalscanurinateearlierthantheycanlactate.Lactationrequir es12monthsforpigs,14monthsforsheepandgoats,and26monthsforcattle,an dlastsfor2monthsforpigs,

6monthsforsheepandgoats,and10monthsforcattle.Theperiodsbetweenlac tationcyclesare2–

6months.Underhormonetreatment,acowproduces10,000Lofmilkperyear comparedto6000Lofurine

Oneofthenegativepointsinproductionofproteinsbytransgenicanimals isthelengthoftimeneededtoassessproductionlevel.Thistakes3.5monthsin mice,15monthsinpigs,28monthsinsheepand

32monthsincows(Chew,1993).Thecostofupkeepofcowsunder

GoodAgriculturalPracticesis$10,000percowperyear

Theproductionofdrugsintransgenicanimalshasbeenstalledbythedemi seofPPLTherapeuticsofScotlandwhich,withtheRoslinInstitute,clonedDo lly,thesheep(Thayer,2003).Theirattempttoproducealungdrugintransgenic sheepforBayerAGwasstoppedandthecompanywasputupforsale

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ansgenicanimals,toproducerecombinantproteinssuchasvaccines,lymp

hokinesetc.Theproductionoftransgenictrypano-somesexpressingheterologousproteinshasseveraladvantagesovertransg

enicanimals.Theseinclude(i)stableandpreciselytargetedintegrationintot

hegenomebyhomologousrecombination,

(ii)achoiceofintegrationintoseveraldefinedsites,allowingexpressionofmul

ti-subunitcomplexes,and(iii)easymaintenanceofcellsinasemi-definedmediumandgrowthtohighdensities(N2 ×107m

l−1)

3.7.Transgenicplants

Forrecombinantproteinproduction,useofplants,ascomparedtothatofl

iveanimalsandanimalcellcultures,ismuchsaferandlessexpensive,requiresl

esstime,andissuperiorintermsofstorageanddistributionissues.Infact,plant

expressionsystemsarebelievedtobeevenbetterthanmicrobesintermsofco

st,proteincomplexity,storageanddistribution.Theuseofplantsoffersanum

berofadvantagesoverotherexpressionsystems(Table6).Thelowriskofcont

aminationwithanimalpathogensincludesvirusessincenoplantvirusesha

vebeenfoundtobepathogenictohumans.Anotheradvantageisthatgrowth

onanagriculturalscalerequiresonlywater,mineralsandsunlight,unlikema

mmaliancellcultivationwhichisanextremelydelicateprocess,veryexpens

ive,requiringbioreactorsthatcostseveralhundredmilliondollarswhenpr

oductionisscaleduptocommerciallevels

Someaddedadvantagesofplantsystemsareglycosylationandtargeting,

compartmentalizationandnaturalstoragestabilityincertainorgans.Simpl

eproteinslikeinterferons,andserumalbuminweresuccessfullyexpressedi

nplantsbetween1986and1990.However,proteinsareoftencomplexthree-dimensionalstructuresrequiringtheproperassemblyoftwoormoresubun

its.Researchersdemonstratedin

1989and1990thatplantswerecapableofexpressingsuchproteinsandassem

blingthemintheiractiveformwhenfunctionalantibodiesweresuccessfully

expressedintransgenicplants.Bacteriadonothavethiscapacity.Transgenic

plantshavebeenusedtoproducevaluableproductssuchasβ-D

-glucuronidase(GUS),avidin,laccaseandtrypsin(Hood,

2002)

Transgenicplantscanbeproducedintwoways.Onewayistoinsertthedesir

edgeneintoavirusthatisnormallyfoundinplants,suchasthetobaccomosaicvi

rusinthetobaccoplant.Theotherwayistoinsertthedesiredgenedirectlyintoth

eplantDNA.Potentialdisadvantagesoftransgenicplantsincludepossiblec

ontaminationwithpesticides,herbicides,andtoxicplantmetabolites(Fitzg

erald,2003)

Productswithtitersashighas0.02–0.2%ofdrycellweighthave

beenachieved.Recombinantproteinshavebeenproducedintransgenic

plantsatlevelsashighas14%oftotaltobaccosolubleprotein(phytasefromA.ni

ger)and1%ofcanolaseedweight(hirudinfromH.medicinalis)

(Kusnadietal.,1997).Oilseedrapeplantscanproduceenkephalinandaneurop

eptide(Sterling,1989).Thepeptidegenewasinsertedintothegeneencodingth

enativestorageproteinbyscientistsatPlantGeneticSystems(Ghent,Belgiu

m).By1997,twoproducts,avidinandGUSwerereadyforthemarket.GUSfrom

E.coliwasproducedincornat0.7%ofsolubleseedprotein.ActivehepatitisBva

ccine(hepatitisBsurfaceantigen)wasproducedintransgenic

Table6

Advantagesoftransgenicplantsasproteinexpressionsystems

Costeffective

Canproducecomplexproteins

HighlevelofaccumulationofproteinsinplanttissuesLowrisk

ofcontaminationwithanimal;pathogensRelativelysimpl

eandcheapproteinpurification

Easyandcheapscaleup

Properfoldingandassemblyofproteincomplexes

Posttranslationalmodifications

tobaccoplants.Despitethesesuccesses,commercialproductionofdrugsint ransgenicplantswassloweddownbytheclosingdownofthePPLTherapeutic s(Thayer,2003),aswellastheexitofMonsantocorporationfromthiseffort 4.Conclusions

Microbeshavebeenusedtoproduceamyriadofprimaryandsecondarypr oductstobenefitmankindformanydecades.Withtheadventofgeneticengi neering,recombinantproteinsenteredthemarket,whichradicallychange dthescenarioofthepharmaceuticalindustry(Demain,2004).Throughtheu seofrecombinantDNA,importantgenes,especiallymammaliangenes,could beamplifiedandclonedinforeignorganisms.Thisprovidedadifferentappro

achtocomplexbiologicalproblem- solving.Manyoftheresultantbiopharmaceuticalsarepro-ducedusingtechnologicallyadvancedmicrobialandmammaliancellbiosys

tems.Thesecell-based,proteinmanufacturingtechnologiesoffermanyadvantages,produci ngrecombinantpharmaceuticallyimportantproteinswhicharesafeandava ilableinabundantsupply

Generally,proteinsthatarelargerthan100kDareexpressedinaeukaryoti csystemwhilethosesmallerthan30kDareexpressedinaprokaryoticsystem

.Forproteinsthatrequireglycosylation,mamma-liancells,fungiorthebaculovirussystemischosen.Theleastexpensive,easiest andquickestexpressionofproteinscanbecarriedoutinE.coli.However,thisba cteriumcannotexpressverylargeproteins.Also,forS–

Srichproteins,andproteinsthatrequirepost-translationalmodifications,E.coliisnotthesystemofchoice,asitcannotcarry outglycosylationandremovetheS–

Ssequences.Sometimes,eukaryoticproteinscanbetoxictobacteria.Yeastsa reeukaryotes,havetheadvantageofgrowingtohighcelldensitiesandarethus

suitableformakingisotopically-labeledproteinsforNMR.ThetwomostutilizedyeastsareS.cerevisiaeandP.pas toris.Yeastscanproducehighyieldsofproteinsatlowcost,proteinslargerthan5 0kDcanbeproduced,signalsequencescanberemoved,andglycosylationcanb ecarriedout.Yeastsproducechaperoninstoassistfoldingofcertainproteinsa ndcanhandleS–

Srichproteins.Thebaculoviralsystemisahighereukaryoticsystemthanyeas

tandcancarryoutmorecomplexpost-translationalmodificationsofproteins.Itprovidesabetterchancetoobtains olubleproteinwhenitisofmammalianorigin,canexpressproteinslargertha n50kDandS–

Srichproteins,cancarryoutglycosylation,removessignalsequences,haschap

er-oninsforfoldingofproteins,ischeapandcanproducehighyieldsofproteins.Th ebaculoviralsystemishoweverslowandtimeconsumingandnotassimpleas yeasts.Themostpopulartypeofsystemforproducingrecombinantmammal ianglycosylatedproteinsisthatofmammaliancells.Theycangenerateprotei nslargerthan50kD,carryoutauthenticsignalsequenceremoval,glycosylate andalsohavechaperonins.Someoftheproteinsexpressedinmammaliansyst

emsareFactorVII,factorIX,γ-interferon,interleukin2,humangrowthhormone,andtPA.However,select ionofcelllinesusuallytakesweeksandthecellcultureissustainableforonlyali mitedtime.Overall,39%ofrecombinantproteinsaremadebyE.coli,35%byCH Ocells,15%byyeasts,10%byothermammaliansystemsand1%byotherbacter iaandothersystems(Rader,2008)

Geneticallymodifiedanimalssuchasthecow,sheep,goat,andrabbitsecre terecombinantproteinsintheirmilk,bloodorurine.Manyusefulbiopharmac euticalscanbeproducedbytransgenicanimalssuchasvaccines,antibodies,a

ndotherbiotherapeutics.Similarly,trans-genicplantssuchasArabidopsisthalianaandotherscangeneratemanyrecomb inantproteins,e.g.,vaccines,bioplastics,andbiotherapeutics.Commerciald evelopmentoftransgenicanimalsandtransgenicplantshasbeenslowhowe ver,comparedtotheabovesystems

Molecularbiologyhasbeenthemajordrivingforceinbiopharma-ceuticalresearchandtheproductionofhighlevelsofproteins.Thebiopharmac euticalindustryismultifaceted,dealingwithribozymes,antisensemolecu les,monoclonalantibodies,genomics,proteomics,

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