Applications of Mass Spectrometry Imaging to Cancer PDF
Preview Applications of Mass Spectrometry Imaging to Cancer
AcademicPressisanimprintofElsevier 50HampshireStreet,5thFloor,Cambridge,MA02139,UnitedStates 525BStreet,Suite1800,SanDiego,CA92101-4495,UnitedStates TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UnitedKingdom 125LondonWall,London,EC2Y5AS,UnitedKingdom Firstedition2017 Copyright©2017ElsevierInc.Allrightsreserved. Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans, electronicormechanical,includingphotocopying,recording,oranyinformationstorageand retrievalsystem,withoutpermissioninwritingfromthepublisher.Detailsonhowtoseek permission,furtherinformationaboutthePublisher’spermissionspoliciesandour arrangementswithorganizationssuchastheCopyrightClearanceCenterandtheCopyright LicensingAgency,canbefoundatourwebsite:www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightby thePublisher(otherthanasmaybenotedherein). Notices Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchand experiencebroadenourunderstanding,changesinresearchmethods,professionalpractices, ormedicaltreatmentmaybecomenecessary. Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgein evaluatingandusinganyinformation,methods,compounds,orexperimentsdescribed herein.Inusingsuchinformationormethodstheyshouldbemindfuloftheirownsafetyand thesafetyofothers,includingpartiesforwhomtheyhaveaprofessionalresponsibility. Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors, assumeanyliabilityforanyinjuryand/ordamagetopersonsorpropertyasamatterof productsliability,negligenceorotherwise,orfromanyuseoroperationofanymethods, products,instructions,orideascontainedinthematerialherein. ISBN:978-0-12-805249-5 ISSN:0065-230X ForinformationonallAcademicPresspublications visitourwebsiteathttps://www.elsevier.com/ Publisher:ZoeKruze AcquisitionEditor:ZoeKruze EditorialProjectManager:FentonCoulthurst ProductionProjectManager:SuryaNarayananJayachandran SeniorCoverDesigner:GregHarris TypesetbySPiGlobal,India CONTRIBUTORS N.Y.R.Agar BrighamandWomen’sHospital;Dana-FarberCancerInstitute,HarvardMedicalSchool, Boston,MA,UnitedStates M.Aichler ResearchUnitAnalyticalPathology,HelmholtzZentrumMu€nchen,Neuherberg,Germany P.M.Angel MedicalUniversityofSouthCarolina,Charleston,SC,UnitedStates G.Arentz AdelaideProteomicsCentre,SchoolofBiologicalSciences;InstituteforPhotonicsand AdvancedSensing(IPAS),UniversityofAdelaide,Adelaide,SA,Australia B.Balluff MaastrichtUniversity,MaastrichtMultiModalMolecularImaginginstitute(M4I), Maastricht,TheNetherlands M.Briggs AdelaideProteomicsCentre,SchoolofBiologicalSciences;InstituteforPhotonicsand AdvancedSensing(IPAS);ARCCentreforNanoscaleBioPhotonics(CNBP),Universityof Adelaide,Adelaide,SA,Australia E.Bruner MedicalUniversityofSouthCarolina,Charleston,SC,UnitedStates A.Buck ResearchUnitAnalyticalPathology,HelmholtzZentrumMu€nchen,Neuherberg,Germany J.Bunch NationalPhysicalLaboratory,Teddington;SchoolofPharmacy,UniversityofNottingham, Nottingham,UnitedKingdom D.Calligaris BrighamandWomen’sHospital,HarvardMedicalSchool,Boston,MA,UnitedStates R.Casadonte ProteopathGmbH,Trier,Germany P.Chaurand Universit(cid:2)edeMontr(cid:2)eal,Montreal,QC,Canada R.R.Drake MedicalUniversityofSouthCarolina,Charleston,SC,UnitedStates M.Dufresne Universit(cid:2)edeMontr(cid:2)eal,Montreal,QC,Canada I.F.Dunn BrighamandWomen’sHospital,HarvardMedicalSchool,Boston,MA,UnitedStates ix x Contributors R.J.A.Goodwin MassSpectrometryImagingGroup,PathologySciences,DrugSafety&Metabolism, InnovativeMedicinesandEarlyDevelopment,AstraZeneca,Cambridge,UnitedKingdom M.Hanselmann HeidelbergCollaboratoryforImageProcessing(HCI),InterdisciplinaryCenterforScientific Computing(IWR),UniversityofHeidelberg,Heidelberg,Germany R.M.A.Heeren MaastrichtUniversity,MaastrichtMultiModalMolecularImaginginstitute(M4I), Maastricht,TheNetherlands Y.-Y.Ho AdelaideProteomicsCentre,SchoolofBiologicalSciences,UniversityofAdelaide, Adelaide,SA,Australia M.K.Hoffmann AdelaideProteomicsCentre,SchoolofBiologicalSciences;InstituteforPhotonicsand AdvancedSensing(IPAS),UniversityofAdelaide,Adelaide,SA,Australia P.Hoffmann AdelaideProteomicsCentre,SchoolofBiologicalSciences;InstituteforPhotonicsand AdvancedSensing(IPAS),UniversityofAdelaide,Adelaide,SA,Australia K.T.Huang BrighamandWomen’sHospital,HarvardMedicalSchool,Boston,MA,UnitedStates K.Huber ResearchUnitAnalyticalPathology,HelmholtzZentrumMu€nchen,Neuherberg,Germany E.E.Jones MedicalUniversityofSouthCarolina,Charleston,SC,UnitedStates J.Kriegsmann ProteopathGmbH;InstituteofMolecularPathology;CenterforHistology,Cytologyand MolecularDiagnostics,Trier,Germany M.Kriegsmann InstituteofPathology,UniversityofHeidelberg,Heidelberg,Germany N.Lauzon Universit(cid:2)edeMontr(cid:2)eal,Montreal,QC,Canada E.Laws BrighamandWomen’sHospital,HarvardMedicalSchool,Boston,MA,UnitedStates R.Longuesp(cid:2)ee ProteopathGmbH,Trier,Germany S.Lou LeidenUniversityMedicalCenter,Leiden,TheNetherlands S.Ludy BrighamandWomen’sHospital,HarvardMedicalSchool,Boston,MA,UnitedStates Contributors xi L.A.McDonnell FondazionePisanaperlaScienzaONLUS,Pisa,Italy;LeidenUniversityMedicalCenter, Leiden,TheNetherlands D.F.McGinnity DMPK,OncologyIMED,InnovativeMedicinesandEarlyDevelopment,AstraZeneca, Cambridge,UnitedKingdom J.S.McKenzie ImperialCollegeLondon,London,UnitedKingdom A.S.Mehta MedicalUniversityofSouthCarolina,Charleston,SC,UnitedStates P.Mittal AdelaideProteomicsCentre,SchoolofBiologicalSciences;InstituteforPhotonicsand AdvancedSensing(IPAS),UniversityofAdelaide,Adelaide,SA,Australia N.H.Patterson MassSpectrometryResearchCenter,VanderbiltUniversitySchoolofMedicine,Nashville, TN,UnitedStates T.W.Powers MedicalUniversityofSouthCarolina,Charleston,SC,UnitedStates S.Santagata BrighamandWomen’sHospital;Dana-FarberCancerInstitute,HarvardMedicalSchool, Boston,MA,UnitedStates K.Schwamborn InstituteofPathology,TechnischeUniversit€atMu€nchen(TUM),Munich,Germany N.Strittmatter DrugSafetyandMetabolism,AstraZeneca,Cambridge,UnitedKingdom Z.Takats ImperialCollegeLondon,London,UnitedKingdom A.Walch ResearchUnitAnalyticalPathology,HelmholtzZentrumMu€nchen,Neuherberg,Germany L.Winderbaum AdelaideProteomicsCentre,SchoolofBiologicalSciences,UniversityofAdelaide, Adelaide,SA,Australia C.Zhang AdelaideProteomicsCentre,SchoolofBiologicalSciences;InstituteforPhotonicsand AdvancedSensing(IPAS),UniversityofAdelaide,Adelaide,SA,Australia PREFACE ItwasthepioneeringworkperformedinthelaboratoryofRichardCaprioli thatledtothecurrentwidespreadapplicationofimagingmassspectrometry tocancerresearch(Caprioli,Farmer,&Gile,1997).Usingspatiallyresolved matrix-assistedlaserdesorption/ionization(MALDIimagingmassspectrom- etry) they demonstrated how the distributions of hundreds of proteins in a tissue section could be simultaneously recorded, without prior knowledge and without labeling. Shortly after this first technical report it was demon- stratedhowthetechniquecouldrevealdifferentialproteinexpressionprofiles throughouttumorsamples,includingproteinslocalizedinthetumor’sinfil- tratingzone(Stoeckli,Chaurand,Hallahan,&Caprioli,2001). Imaging mass spectrometry has grown rapidly, in terms of application andtechnology.Newtechnologiesnowenablehighspeed,highspatialres- olution, and high mass resolution analysis; new tissue preparation methods enable the label-free analysis of diverse molecular classes, including hor- mones,peptides,proteins,proteinisoforms(Chapter2),lipids(Chapter3), glycans(Chapter4),metabolites(Chapter5),anddrugs(aswellasthedrug’s metabolites)(Chapter6);newdataregistrationmethodsenabletheseamless integration of imaging mass spectrometry with histopathological analysis andinvivoimaging,inbothtwoandthreedimensions;andfinallynewdata analysisroutineshaveenabledallofthesetoolstobeusedtoinvestigatethe molecular changes that accompany cancer development. While earlier applications of imaging mass spectrometry focused on the identification of diagnosticbiomarkers,thetechniquehasdevelopedrapidlyandisnowused toidentifybiomarkersofsurvival,metastaticstatus,hormonereceptorstatus, microvascularinvasion,andpatientresponsetotherapy;thetechniqueisalso used to investigate intratumor heterogeneity, from tumor cell density, tumorcelltype,andevensubpopulationphenotypeperspectives(Chapter8), and intraoperatively to rapidly assess tumor margins during surgery (Chapters 9 and 10). In part the developments in imaging mass spectrometry reflect the demandsoftheapplicationareas,aswellastheactiveinvolvementofscien- tists from different disciplines. Pharmaceutical analysis (Chapter 6) is now established as one of the principal application areas of imaging mass spectrometry owing to its ability to help reduce the cost of developing and testing new drugs and drug formulations. xiii xiv Preface The active involvement of pathologists in the application of imaging mass spectrometry is of paramount importance (Chapters 1 and 7); it is thecombinationofhistologyandimagingmassspectrometry,enablingmass spectralprofilesofspecifichistopathologicalfeaturestobeobtained,thatis, theuniquestrengthofthetechniqueforcancerresearch.Inthisissueaseries ofreviewscoverhowthetechniquecanbeappliedincancerresearch,both fromadiagnosticandbiologicalperspective.Thewidearrayofbiomolecular targets central to cancer development and progression that can be detected in cancer tissues and emerging applications of imaging mass spectrometry technology are also evaluated. RICHARD R. DRAKE LIAM A. MCDONNELL REFERENCES Caprioli,R.M.,Farmer,T.B.,&Gile,J.(1997).Molecularimagingofbiologicalsamples: LocalizationofpeptidesandproteinsusingMALDI-TOFMS.AnalyticalChemistry,69, 4751–4760. Stoeckli, M., Chaurand, P., Hallahan, D. E., & Caprioli, R. M. (2001). Imaging mass spectrometry: A new technology for the analysis of protein expression in mammalian tissues.NatureMedicine,7,493–496. CHAPTER ONE The Importance of Histology and Pathology in Mass Spectrometry Imaging K. Schwamborn1 InstituteofPathology,TechnischeUniversit€atMu€nchen(TUM),Munich,Germany 1Correspondingauthor:e-mailaddress:[email protected] Contents 1. ImportanceofPathology 2 2. PossibleErrorsCausedbyTissueInherentFactors—WhyHistologyIsImportant forSupervisedAnalysis 4 3. PossibleErrorsCausedbySampleInherentFactors—SmallPretherapeutic Biopsies 9 4. PossibleErrorsCausedbySamplePreparations—ArtifactsAreNotYourFriend 12 5. PossibleErrorsCausedbyIll-DefinedSampleGroupsintheTrainingSet—KeepIt BlackandWhite/ShadesofGrayAreNotWelcome 16 6. Conclusion 19 References 20 Abstract Massspectrometryimaging(MSI)hasbecomeavaluabletoolincancerresearch.Even more,duetoitscapabilitytodirectlylinkmolecularchangeswithhistology,itholdsthe prospecttorevolutionizetissue-baseddiagnostics.Inordertolearntowalkbeforerun- ning, however, information obtained through classical histology should not be neglectedbutratherusedtoitsfullcapacityandintegratedwithmassspectrometry data to lead to a superior molecular histology synthesis. In order to achieve this, pathomorphological analyseshavetobeintegrated intoMSIanalysesrightfromthe beginningtoavoiderrorsandpitfallsofMSIapplicationpossiblyleadingtoincorrect orimprecisestudyoutcomes.Sucherrorscanbecausedbydifferentsampleortissue inherentfactorsorthroughfactorsinsamplepreparation.Futurestudiesshould,there- fore,aimforacomprehensiveincorporationofhistologyandpathologycharacteristics toensurethegenerationofhigh-qualitydatainMSItoexploititsfullcapacityintissue- basedbasicandtranslationalresearch. AdvancesinCancerResearch,Volume134 #2017ElsevierInc. 1 ISSN0065-230X Allrightsreserved. http://dx.doi.org/10.1016/bs.acr.2016.11.001 2 K.Schwamborn 1. IMPORTANCE OF PATHOLOGY The old saying that “a picture is worth a thousand words” is doubt- lesslyalsotrueinscience.Interpretationofhistomorphologicalchangeshas substantially contributed to the understanding of physiological and patho- logicalbiologicalprocessesindifferentorgans.Recently,however,thefocus hasshiftedtowardaddingadditionalmolecularcomponentstosuchconven- tionalimagingtechniques.Thisso-calledmolecularhistologyissupposedto reveal the underlying biochemistry of tissues and organs, while simulta- neously providing additional information on how therapeutics or toxins influencethefunctionormisfunctionofanorgan(Vachet,2015).However, correct interpretation of these molecular “pictures” can only be done in conjunction with simultaneous interpretation of the underlying conven- tional histomorphological “picture” by trained pathologists/morphologist. Having a profound knowledge and understanding of the biological basis of disease is the key for correct interpretation of tissue phenotypes. While, forexample,biologistandotherscientistscanfulfilsomeofthoseneeds,only a trained pathologist/morphologist is able to integrate the morphological, clinical,andmoleculardimensionsofastudieddisease.Abiologistcancer- tainlylearnspecificmorphologyinterpretationinselected(patho)physiolog- icalsettings;however,forafullscalecomprehensiveinterpretationusuallya trainedanatomistorpathologistisneeded,whohastrainedontheinterpre- tationofthewholespectrumofpossiblehistomorphologicaltissuechanges overseveralyears/decades.Nevertheless,sinceonlyafewtrainedmorphol- ogistsarededicatedtoresearchandevenlessareworkinginthefieldofmass spectrometryimaging(MSI),theinterfacebetweenbasicresearchanddiag- nosticmorphologyisprobablytheweakestlinkinthewholeinterpretation chaininmolecularimaging.Ithasbecomeevident,however,thatinorder toadvancethetranslationofbiomarkerdiscoveryintodiagnosticandther- apeuticapplication,morphologistsandespeciallypathologistshavetoplaya major role in this endeavor (Salto-Tellez, James, & Hamilton, 2014). Histology, the study of the microscopic structure of tissues, is an integral part of daily pathology routine. According to the Oxford English Dictionary, pathology is the science of the causes and effects of diseases (Stevenson,2010);inparticular,however,theterm“pathology”alsostands forasubspecialtyofmedicinethatdealswiththelaboratoryexaminationof samplesofbodytissuesfordiagnosticpurposes(Stevenson,2010).Pathology bridges science and medicine and underpins every aspect of patient care, ApplicationsofMassSpectrometryImagingtoCancer 3 from diagnostic testing, quality control, and treatment advice to the use of cutting-edgegenetictechnologies andthepreventionofdisease.Theanal- ysisofcytology,biopsy,orresectionspecimenoftenrepresentsthefinalstep indiagnosticprocessesandhasremainedthelinchpinofcancerdiagnosisfor over 100 years (Lakhani & Ashworth, 2001). This knowledge provides a vitalservice;thepathologyreportisintendedtoguidethephysicianinfind- ingtheoptimaltreatment foraparticular patientandbuildstheframework for future selection of new markers and new therapies for a given patient. In the era of individualized medicine, standard clinical care is continu- ously becoming more complex, resulting in more complex and extensive diagnosticpathology workup. Thisbecomes obviousby comparingguide- lines for tissuepreparationof lungcancer surgical specimens,wheresimple histochemistrystainssuchashematoxylinandeosinandperiodicacid–Schiff stain were sufficient in the 1960s. In contrast, today’s pathology workup requires a plethora of additional information, including subtyping based on a number of immunohistochemical stains, semiquantitative assessment of growth pattern in the case of a pulmonary adenocarcinoma, and often additional molecular analyses. The increasing complexity in pathology workupisalsoreflectedbyamorethan60%increaseinthenumberoftissue blockspercaseandslidespertissueblockoverthelastdecade(e.g.,immu- nohistochemistry and PCR) (Warth et al., 2016). Especially in the field of oncology, cell- and tissue-related molecular diagnostics results from tech- niquesincludingimmunohistochemistry,fluorescenceinsituhybridization, and extraction-based molecular diagnostics such as PCR and sequencing today determine therapy decisions. And although extraction-based molec- ular diagnostics such as PCR and sequencing are molecular tests, they still strongly rely on an initial pathological examination of tissue samples to ensure sample adequacy, correct annotation of tumor areas for possible tumorcellenrichment,togetherwithestimationofthetumorcellpercent- age.Inparticular,thepercentageoftumorcellswithinagivenareaselected forextractionwillultimatelydeterminetheyieldandpossible“dilution”of tumorDNAbyothercelltypeswhichisessentialfortheinterpretationand accuracy of molecular test results. Consequently, inadequate sampling can result in a false-negative test result due to insufficient tumor DNA yield andultimatelyinthewrongtherapy(Thunnissenetal.,2012).Thus,correct aprioriinterpretationandannotationoftissuemorphologybypathologistsis key for the correct outcome of molecular testing. Alongthesameline,pathologicalevaluationisalsoofutmostimportance in MALDI imaging. This is obvious in all histology-directed approaches 4 K.Schwamborn where only small predefined areas of a sample are analyzed (Cornett et al., 2006).However,histologycoannotationisalsoofparamountimportancein allotherMSIapproaches.Possiblepitfallscausedbyinexperience,explana- tions, and solutions will be given within the following paragraphs. 2. POSSIBLE ERRORS CAUSED BY TISSUE INHERENT FACTORS—WHY HISTOLOGY IS IMPORTANT FOR SUPERVISED ANALYSIS With the advent and rise of molecular biology predictions on substituting histological assessment with molecular analyses were made. However, until now traditional microscopic morphological tissue analysis isstillthegoldstandardandtheconditiosinequanonforsubsequentmolec- ular testing. The rationale behind that fact is the need for high-quality microscopic tissue analysis prior to any other molecular test to establish adequacy of the sample (Szasz, Gyorffy, & Marko-Varga, 2016). Thereisanequivalentneedforhigh-qualityhistologicalexaminationin mass spectrometry imaging, in particular in studies with supervised data analysis.Thesetypesofstudiestypicallyaimtounraveldifferencesbetween two or more different sample sets, e.g., normal and diseased tissue or two different subtypes of disease. Thus, in order to ensure, sample adequacy severalfactorshavetobeconsidered.Firstofall,ithastobeestablishedthat thesamplerepresentstherighthistologicaltypefortheintendedanalysisand is representative of the underlying disease. Second, the number of disease- defining cells within a given area has to be sufficient and above the detec- tion/sensitivitylimitoftheanalysis.Additionally,thereshouldbenomajor interfering cell component (e.g., inflammatory cells or red blood cells) withinthetissueareaofinterestandnostrongmorphologicalheterogeneity. To exclude samples with inadequate preanalytical conditions, features suggestingthesamplehasbeencompromised(e.g.,autolysis)havetoberec- ognized.Theseandmanyotheraspectsofhistomorphologicalinterpretation oftissuesamplesrepresentanessentialfirststeptoensuretheinterpretability ofthesubsequentimagingmassspectrometryexperiment.Onlycorrectand precise annotation can lead to valid, robust, and meaningful data. In the following paragraphs, these aspects will be discussed in detail using the example of cancer. Whencomparingdifferenttumortypes,itisobviousthatthesamplehas to contain tumor cells. On the other hand, when comparing tumor and
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