Nanopore Technology: Methods and Protocols PDF
Preview Nanopore Technology: Methods and Protocols
Methods in Molecular Biology 2186 Monifa A.V. Fahie Editor Nanopore Technology Methods and Protocols M M B ETHODS IN OLECULAR IO LO GY SeriesEditor JohnM.Walker School of Lifeand MedicalSciences University ofHertfordshire Hatfield, Hertfordshire, UK Forfurther volumes: http://www.springer.com/series/7651 For over 35 years, biological scientists have come to rely on the research protocols and methodologiesinthecriticallyacclaimedMethodsinMolecularBiologyseries.Theserieswas thefirsttointroducethestep-by-stepprotocolsapproachthathasbecomethestandardinall biomedicalprotocolpublishing.Eachprotocolisprovidedinreadily-reproduciblestep-by- step fashion, opening with an introductory overview, a list of the materials and reagents neededtocompletetheexperiment,andfollowedbyadetailedprocedurethatissupported with a helpful notes section offering tips and tricks of the trade as well as troubleshooting advice. These hallmark features were introduced by series editor Dr. John Walker and constitutethekeyingredientineachandeveryvolumeoftheMethodsinMolecularBiology series. Tested and trusted, comprehensive and reliable, all protocols from the series are indexedinPubMed. Nanopore Technology Methods and Protocols Edited by Monifa A. V. Fahie Molecular and Cellular Biology Program, University of Massachusetts Amherst, Amherst, MA, USA Editor MonifaA.V.Fahie MolecularandCellularBiology Program UniversityofMassachusettsAmherst Amherst,MA,USA ISSN1064-3745 ISSN1940-6029 (electronic) MethodsinMolecularBiology ISBN978-1-0716-0805-0 ISBN978-1-0716-0806-7 (eBook) https://doi.org/10.1007/978-1-0716-0806-7 ©SpringerScience+BusinessMedia,LLC,partofSpringerNature2021 AllrightsarereservedbythePublisher,whetherthewholeorpartofthematerialisconcerned,specificallytherightsof translation,reprinting,reuseofillustrations,recitation,broadcasting,reproductiononmicrofilmsorinanyotherphysical way,andtransmissionorinformationstorageandretrieval,electronicadaptation,computersoftware,orbysimilaror dissimilarmethodologynowknownorhereafterdeveloped. Theuseofgeneraldescriptivenames,registerednames,trademarks,servicemarks,etc.inthispublicationdoesnotimply, evenintheabsenceofaspecificstatement,thatsuchnamesareexemptfromtherelevantprotectivelawsandregulations andthereforefreeforgeneraluse. Thepublisher,theauthors,andtheeditorsaresafetoassumethattheadviceandinformationinthisbookarebelievedto betrueandaccurateatthedateofpublication.Neitherthepublishernortheauthorsortheeditorsgiveawarranty, expressedorimplied,withrespecttothematerialcontainedhereinorforanyerrorsoromissionsthatmayhavebeen made.Thepublisherremainsneutralwithregardtojurisdictionalclaimsinpublishedmapsandinstitutionalaffiliations. ThisHumanaimprintispublishedbytheregisteredcompanySpringerScience+BusinessMedia,LLCpartofSpringer Nature. Theregisteredcompanyaddressis:1NewYorkPlaza,NewYork,NY10004,U.S.A. Preface Thefieldofnanoporetechnologyforsinglemoleculesensinghasgarneredmuchattention with its robust application in DNA sequencing. Much effort over the last two decades in nanoporedesign and computationalanalysishasmadenanopore-based DNAsequencinga real-world (and outer space) technique, not only used in the confines of a research labora- tory.Nanoporesensing,however,isalsousedfor theanalysisofotherbiologicalmolecules suchasRNAandproteinsaswellaschemicalssuchasmetabolites,toxins,ordrugs. Inrecentyears,interestinproteinanalysisandpeptidesequencinghasgainedtractionin andamongthemembersofthenanoporetechnologyfield.However,unlikeDNAandRNA sequencing, precise and accurate protein analysis has several obstacles. Therefore, this volumeprimarilyfocusesonafewofthesinglemoleculemethodsandnanoporesdeveloped for thespecificandselectivecharacterizationofproteinanalytes. Nanopores are nanometer-sized holes. In nature, small holes exist as membrane chan- nels that act as gatekeepers, allowing or disallowing molecules to enter or exit the cell. Membrane channels exist in all forms of life. It is here where the field of nanopore technology gained inspiration from as far back as in the 1980s, where the intrinsic activity of acetylcholine receptors were being studied or the nonspecific activity of voltage- dependent anion channels (VDAC) against synthetic molecules were studied in model lipid bilayers [1, 2]. Not only are nanopores based on protein channels but also solid-state materials and synthetic DNA origami. Solid-state nanopores, although not represented in thisbook,areaclassofnanoporesthathaveshowngreatpromiseinproteinanalysis[3–6]. Theadvantageofsyntheticnanoporesistheoptionofsizetunabilitywhiletheadvantageof purifiedproteinnanoporesisconsistentandpreciseporecharacteristicssuchasdiameterand asymmetric charge distribution. Hybrid nanopores combine both biological and synthetic nanoporesandareadevelopingtechniquethatcanpushtheboundariesofproteinanalysis bysinglenanoporesensingtechnology. Nanopore sensing is performed in either one of three main strategies. Firstly, early nanopore research focused heavily on the passage of analytes through the nanopore’s lumen, a process called translocation. Molecules upon entering the nanopore lumen would displace water and, therefore, block ion movement through the pore, resulting in a measurabledecreaseinioniccurrent.Thesizeofthecurrentblockagesiscongruentwiththe molecular weightorsizeofthetranslocatingmolecule.Currently,thisdetectionmethodis primarilyusedbysolid-statenanoporesbutalsousedbyproteinnanopores,asexampledin Chapters3–6,10,11,and13–15. Inrecentyears,othermethodsofanalytedetectionbyproteinnanoporeshavebecome popular. For example, analyte trapping, which can be considered as incomplete transloca- tion,hasonly beensuccessfully performed withproteinnanopores withasymmetric lumen characteristics and constriction sites significantly smaller than the rest of the lumen, i.e., goblet-shapednanopores.Oneexample,thecytolysinA(ClyA)nanoporehasbeenusedto trapproteinanalytesupto~40kDainsize[7,8].Theproteinanalytes’behaviorinsidethe ClyAnanoporecangiveinformationaboutitscompactnessorrigidityandcanalsoreporton conformationalchangesduetoligand–proteininteractions. Finally,proteinnanoporescanalsodetectanalytesthatdonotenteritslumenbutthose that interact with an external binding site that is either intrinsic to the nanopore or that v vi Preface which has been engineered. Chapters 7–9 give detailed methodologies for this type of nanoporedetectionsystem. This book, with its focus on nanopore technology and biomolecule characterization, will hold the interest of the biophysicists, biochemists, bioengineers, and molecular biolo- gists among us. This book’s contributions come from a collective of 39 scientists from all over the world, working diligently in this growing field of nanopore sensing application. Thisbookincludes16chapterswhicharegroupedintofourparts: PartIconsistsoffourchapterswhichlaytheframeworkforthefoundationofnanopore technology:nanoporedesignandnanoporeproduction. Part II consists of seven chapters discussing various biological nanopores, nanopore engineering,andtheir usesinsinglemoleculesensing.Inparticular,thesensingof proteinsandoneexampleofsugarsensingareoutlined. Part III consists of two chapters outlining computational methods to study intrinsic nanopore behavior as well asthe formulationsfor characterizingthe specific trans- locationactivityofavesicleparticlethroughananopore. PartIVconsistsofthreechaptersspecificallydetailingtheuseofthetechniquedroplet interfacebilayer(DIB)innanoporeandmembranebiophysicalstudies. Theeditor wishestothankallthecontributorsfortheirdedicationandpatienceduring thecreationofthisbook. Amherst,MA,USA MonifaA.V.Fahie References 1. Suarez-Isla BA, Wan K, Lindstrom J, Montal M (1983) Single-channel recordings from purified acetylcholine receptors reconstituted in bilayers formed at the tip of patch pipets. Biochemistry 22:2319–2323 2. ZimmerbergJ,ParsegianVA(1986)Polymerinaccessiblevolumechangesduringopeningandclosing ofavoltage-dependentionicchannel.Nature323:36–39 3. HanA,Schu¨rmannG,MondinG,BitterliRA,HegelbachNG,DeRooijNF,StauferU(2006)Sensing proteinmoleculesusingnanofabricatedpores.ApplPhysLett88:1–4 4. FologeaD,LeddenB,McNabbDS,LiJ(2007)Electricalcharacterizationofproteinmoleculesbya solid-statenanopore.ApplPhysLett91:53901-1–53901-3 5. TalagaDS,LiJ(2009)Single-moleculeproteinunfoldinginsolidstatenanopores.JAmChemSoc 131:9287–9297 6. NirI,HuttnerD,MellerA(2015)Directsensinganddiscriminationamongubiquitinandubiquitin chainsusingsolid-statenanopores.BiophysJ108:2340–2349 7. MeerveltVVan,SoskineM,MagliaG(2014)Detectionoftwoisomericbindingconfigurationsina proteinaptamercomplexwithabiologicalnanopore.ACSNano8:12826–12835 8. Willems K, Ruic´ D, Biesemans A, Galenkamp NS, Van Dorpe P, Maglia G (2019) Engineering and modelingtheelectrophoretictrappingofasingleproteininsideananopore.ACSNano13:9980–9992 Contents Preface ..................................................................... v Contributors................................................................. ix PART I DESIGN AND PREPARATION OF BIOLOGICAL BASED NANOPORES 1 PreparationofFragaceatoxinC(FraC)Nanopores.......................... 3 NatalieLisaMutter,GangHuang,NieckJordyvanderHeide, FlorianLeonardusRudolfusLucas,NicoleSte´phanieGalenkamp, GiovanniMaglia,andCarstenWloka 2 PreparationofCytolysinA(ClyA)Nanopores .............................. 11 NicoleSte´phanieGalenkamp,VeerleVanMeervelt,NatalieLisaMutter, NieckJordyvanderHeide,CarstenWloka,andGiovanniMaglia 3 BuildingSyntheticTransmembranePeptidePores .......................... 19 KozhinjamparaR.Mahendran 4 DesignandAssemblyofMembrane-SpanningDNANanopores.............. 33 KerstinG¨opfrich,AlexanderOhmann,andUlrichF.Keyser PART II SINGLE MOLECULE DETECTION AND ANALYSIS OF PROTEIN ANALYTES 5 DeterminingtheOrientationofPorinsinPlanarLipidBilayers............... 51 SandraA.Ionescu,SejeongLee,andHaganBayley 6 RevelationofFunctionandInhibitionofWzaThrough Single-ChannelStudies .................................................. 63 LingbingKong 7 ProteinAnalyteSensingwithanOuterMembraneProteinG (OmpG)Nanopore ..................................................... 77 MonifaA.V.Fahie,BibYang,ChristinaM.Chisholm,andMinChen 8 NanoporeEnzymologytoStudyProteinKinasesandTheir InhibitionbySmallMolecules............................................ 95 LeonHarrington,LeilaT.Alexander,StefanKnapp, andHaganBayley 9 ASelectiveActivity-BasedApproachforAnalysisofEnzymes withanOmpGNanopore................................................ 115 MonifaA.V.Fahie,BachPham,FanjunLi,andMinChen 10 Oligonucleotide-DirectedProteinThreadingThrougha RigidNanopore ........................................................ 135 Garbin˜eCelayaandDavidRodriguez-Larrea 11 UnfoldingandTranslocationofProteinsThroughan Alpha-HemolysinNanoporebyClpXP .................................... 145 JeffNivala,LoganMulroney,QingLuan,RobinAbu-Shumays, andMarkAkeson vii viii Contents PART III COMPUTATIONAL ANALYSIS OF NANOPORE BEHAVIOR 12 SimulationofpH-Dependent,Loop-BasedMembraneProtein GatingUsingPretzel.................................................... 159 AlanPerez-Rathke,MonifaA.V.Fahie,ChristinaM.Chisholm, MinChen,andJieLiang 13 FreeEnergyMinimizationforVesicleTranslocationThrough aNarrowPore.......................................................... 171 HamidR.Shojaei,AhadKhaleghiArdabili,and MurrugappanMuthukumar PART IV DROPLET INTERFACE BILAYER SYSTEM 14 SingleIon-ChannelAnalysisinDropletInterfaceBilayer .................... 187 ArashManafirad 15 ContinuousandRapidSolutionExchangeinaLipidBilayer PerfusionSystemBasedonDroplet-InterfaceBilayer........................ 197 En-HsinLee 16 ProteinTransportStudiedbyaModelAsymmetricMembrane ArmyArrangedinaDimpleChip......................................... 213 XinLiandMinChen Index ...................................................................... 227 Contributors ROBINABU-SHUMAYS • UCSantaCruzGenomicsInstitute,UniversityofCalifornia,Santa Cruz,SantaCruz,CA,USA MARKAKESON • UCSantaCruzGenomicsInstitute,UniversityofCalifornia,SantaCruz, SantaCruz,CA,USA LEILAT.ALEXANDER • NuffieldDepartmentofClinicalMedicine,StructuralGenomics ConsortiumandTargetDiscoveryInstitute,UniversityofOxford,Oxford,UK; PersonalizedHealthInformatics,SIBSwissInstituteofBioinformatics,Basel,Switzerland HAGANBAYLEY • DepartmentofChemistry,UniversityofOxford,Oxford,UK GARBIN˜ECELAYA • DepartmentofBiochemistryandMolecularBiology(UPV/EHU), BiofisikaInstitute(CSIC,UPV/EHU),Leioa,Spain MINCHEN • DepartmentofChemistry,UniversityofMassachusettsAmherst,Amherst,MA, USA CHRISTINA M.CHISHOLM • MolecularandCellularBiologyProgram,Universityof MassachusettsAmherst,Amherst,MA,USA MONIFAA.V.FAHIE • MolecularandCellularBiologyProgram,UniversityofMassachusetts Amherst,Amherst,MA,USA NICOLESTE´PHANIEGALENKAMP • GroningenBiomolecularSciencesandBiotechnology Institute,UniversityofGroningen,Groningen,TheNetherlands KERSTIN GO¨PFRICH • CavendishLaboratory,UniversityofCambridge,Cambridge,UK LEON HARRINGTON • DepartmentofChemistry,UniversityofOxford,Oxford,UK;Max PlanckInstituteofBiochemistry,Martinsried,Germany GANGHUANG • GroningenBiomolecularSciencesandBiotechnologyInstitute,Universityof Groningen,Groningen,TheNetherlands SANDRA A.IONESCU • DepartmentofChemistry,UniversityofOxford,Oxford,UK ULRICHF.KEYSER • CavendishLaboratory,UniversityofCambridge,Cambridge,UK AHADKHALEGHIARDABILI • SchoolofEngineeringandNaturalSciences,Altınbas¸ University,Istanbul,Turkey STEFANKNAPP • NuffieldDepartmentofClinicalMedicine,StructuralGenomics ConsortiumandTargetDiscoveryInstitute,UniversityofOxford,Oxford,UK;Institute forPharmaceuticalChemistry,StructuralGenomicsConsortium,andBuchmannInstitute forMolecularLifeSciences,JohannWolfgangGoethe-University,FrankfurtamMain, Germany LINGBINGKONG • InternationalInstituteofRareSugarResearchandEducation, DepartmentofAppliedBiologicalScience,FacultyofAgriculture,KagawaUniversity, Miki,Kagawa,Japan EN-HSINLEE • DepartmentofChemistry,UniversityofMassachusettsAmherst,Amherst, MA,USA SEJEONGLEE • DepartmentofChemistry,UniversityofOxford,Oxford,UK JIELIANG • DepartmentofBioengineering,UniversityofIllinoisatChicago,Chicago,IL, USA FANJUN LI • DepartmentofChemistry,UniversityofMassachusettsAmherst,Amherst,MA, USA XINLI • DepartmentofChemistry,UniversityofMassachusettsAmherst,Amherst,MA,USA ix
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