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Hallmarks of cancer the next generation

Review

HallmarksofCancer:TheNextGeneration

DouglasHanahan1,2,*andRobertA.Weinberg3,*

SwissInstituteforExperimentalCancerResearch(ISREC),SchoolofLifeSciences,EPFL,LausanneCH-1015,SwitzerlandDepartmentofBiochemistry&Biophysics,UCSF,SanFrancisco,CA94158,USA

3WhiteheadInstituteforBiomedicalResearch,Ludwig/MITCenterforMolecularOncology,andMITDepartmentofBiology,Cambridge,MA02142,USA

*Correspondence:dh@ep .ch(D.H.),weinberg@wi.mit.edu(R.A.W.)DOI10.1016/j.cell.2011.02.013

2The1The

LeadingEdge

Thehallmarksofcancercomprisesixbiologicalcapabilitiesacquiredduringthemultistepdevelop-mentofhumantumors.Thehallmarksconstituteanorganizingprincipleforrationalizingthecomplexitiesofneoplasticdisease.Theyincludesustainingproliferativesignaling,evadinggrowthsuppressors,resistingcelldeath,enablingreplicativeimmortality,inducingangiogenesis,andacti-vatinginvasionandmetastasis.Underlyingthesehallmarksaregenomeinstability,whichgeneratesthegeneticdiversitythatexpeditestheiracquisition,andin ammation,whichfostersmultiplehall-markfunctions.Conceptualprogressinthelastdecadehasaddedtwoemerginghallmarksofpotentialgeneralitytothislist—reprogrammingofenergymetabolismandevadingimmunedestruction.Inadditiontocancercells,tumorsexhibitanotherdimensionofcomplexity:theycontainarepertoireofrecruited,ostensiblynormalcellsthatcontributetotheacquisitionofhall-marktraitsbycreatingthe‘‘tumormicroenvironment.’’Recognitionofthewidespreadapplicabilityoftheseconceptswillincreasinglyaffectthedevelopmentofnewmeanstotreathumancancer.

INTRODUCTION

Wehaveproposedthatsixhallmarksofcancertogetherconsti-tuteanorganizingprinciplethatprovidesalogicalframeworkforunderstandingtheremarkablediversityofneoplasticdiseases(HanahanandWeinberg,2000).Implicitinourdiscussionwasthenotionthatasnormalcellsevolveprogressivelytoaneoplasticstate,theyacquireasuccessionofthesehallmarkcapabilities,andthatthemultistepprocessofhumantumorpathogenesiscouldberationalizedbytheneedofincipientcancercellstoacquirethetraitsthatenablethemtobecometumorigenicandultimatelymalignant.

Wenotedasanancillarypropositionthattumorsaremorethaninsularmassesofproliferatingcancercells.Instead,theyarecomplextissuescomposedofmultipledistinctcelltypesthatparticipateinheterotypicinteractionswithoneanother.Wede-pictedtherecruitednormalcells,whichformtumor-associatedstroma,asactiveparticipantsintumorigenesisratherthanpassivebystanders;assuch,thesestromalcellscontributetothedevelopmentandexpressionofcertainhallmarkcapabilities.Duringtheensuingdecadethisnotionhasbeensolidi edandextended,revealingthatthebiologyoftumorscannolongerbeunderstoodsimplybyenumeratingthetraitsofthecancercellsbutinsteadmustencompassthecontributionsofthe‘‘tumormicroenvironment’’totumorigenesis.

Inthecourseofremarkableprogressincancerresearchsubsequenttothispublication,newobservationshaveservedbothtoclarifyandtomodifytheoriginalformulationofthehall-markcapabilities.Inaddition,yetotherobservationshaveraisedquestionsandhighlightedmechanisticconceptsthatwerenotintegraltoouroriginalelaborationofthehallmarktraits.Moti-646Cell144,March4,2011ª2011ElsevierInc.

vatedbythesedevelopments,wenowrevisittheoriginalhall-marks,considernewonesthatmightbeincludedinthisroster,andexpanduponthefunctionalrolesandcontributionsmadebyrecruitedstromalcellstotumorbiology.

HALLMARKCAPABILITIES—CONCEPTUALPROGRESSThesixhallmarksofcancer—distinctiveandcomplementarycapabilitiesthatenabletumorgrowthandmetastaticdissemina-tion—continuetoprovideasolidfoundationforunderstandingthebiologyofcancer(Figure1;seetheSupplementalInforma-tionfordownloadableversionsofthe guresforpresentations).Inthe rstsectionofthisReview,wesummarizetheessenceofeachhallmarkasdescribedintheoriginalpresentationin2000,followedbyselectedillustrations(demarcatedbysub-headingsinitalics)oftheconceptualprogressmadeoverthepastdecadeinunderstandingtheirmechanisticunderpinnings.Insubsequentsectionsweaddressnewdevelopmentsthatbroadenthescopeoftheconceptualization,describinginturntwoenablingcharacteristicscrucialtotheacquisitionofthesixhallmarkcapabilities,twonewemerginghallmarkcapabilities,theconstitutionandsignalinginteractionsofthetumormicroen-vironmentcrucialtocancerphenotypes,andwe nallydiscussthenewfrontieroftherapeuticapplicationoftheseconcepts.SustainingProliferativeSignaling

Arguablythemostfundamentaltraitofcancercellsinvolvestheirabilitytosustainchronicproliferation.Normaltissuescarefullycontroltheproductionandreleaseofgrowth-promotingsignalsthatinstructentryintoandprogressionthroughthecellgrowth-and-divisioncycle,therebyensuringahomeostasisofcell

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