c-di-GMP signaling : methods and protocols

477 Pages·2017·11.249 MB·English

by  Sauer, Karin

Methods in
Molecular Biology 1657
Karin Sauer Editor
c-di-GMP
Signaling
Methods and Protocols
M M B
ETHODS IN OLECULAR IO LO GY
SeriesEditor
JohnM.Walker
School of Lifeand MedicalSciences
University ofHertfordshire
Hatfield, Hertfordshire,AL109AB,UK
Forfurther volumes:
http://www.springer.com/series/7651
c-di-GMP Signaling
Methods and Protocols
Edited by
Karin Sauer
Department of Biological Sciences
Binghamton University
Binghamton, NY, USA
Editor
KarinSauer
DepartmentofBiologicalSciences
BinghamtonUniversity
Binghamton,NY,USA
ISSN1064-3745 ISSN1940-6029 (electronic)
MethodsinMolecularBiology
ISBN978-1-4939-7239-5 ISBN978-1-4939-7240-1 (eBook)
DOI10.1007/978-1-4939-7240-1
LibraryofCongressControlNumber:2017943962
©SpringerScience+BusinessMediaLLC2017
Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpartofthematerialis
concerned,specificallytherightsoftranslation,reprinting,reuseofillustrations,recitation,broadcasting,reproduction
onmicrofilmsorinanyotherphysicalway,andtransmissionorinformationstorageandretrieval,electronicadaptation,
computersoftware,orbysimilarordissimilarmethodologynowknownorhereafterdeveloped.
Theuseofgeneraldescriptivenames,registerednames,trademarks,servicemarks,etc.inthispublicationdoesnotimply,
evenintheabsenceofaspecificstatement,thatsuchnamesareexemptfromtherelevantprotectivelawsandregulations
andthereforefreeforgeneraluse.
Thepublisher,theauthorsandtheeditorsaresafetoassumethattheadviceandinformationinthisbookarebelievedto
betrueandaccurateatthedateofpublication.Neitherthepublishernortheauthorsortheeditorsgiveawarranty,
expressorimplied,withrespecttothematerialcontainedhereinorforanyerrorsoromissionsthatmayhavebeenmade.
Thepublisherremainsneutralwithregardtojurisdictionalclaimsinpublishedmapsandinstitutionalaffiliations.
Printedonacid-freepaper
ThisHumanaPressimprintispublishedbySpringerNature
TheregisteredcompanyisSpringerScience+BusinessMediaLLC
Theregisteredcompanyaddressis:233SpringStreet,NewYork,NY10013,U.S.A.
Preface
Fromtherelativeobscurityofanallostericactivatorofabacterialcellulosesynthase,dimeric
(30 ! 50) GMP (cyclic di-GMP or c-di-GMP) has emerged as one of the most common,
important,andtrulyuniversalbacterialsecondmessengers.Cyclicdi-GMPplayskeyrolesin
lifestyle changes of many bacteria, including transition from the planktonic to the sessile
lifestyle,whichaidsintheestablishmentofmulticellularbiofilmcommunities,andfromthe
virulentstateinacuteinfectionstothelessvirulentbutmoreresilientstatecharacteristicof
chronic infectious diseases. C-di-GMP has also been shown to regulate motility, the cell
cycle,anddifferentiationandtoparticipateininterkingdomsignaling,withc-di-GMPbeing
recognizedbymammalianimmunesystemsasauniquelybacterialmolecule.Modulatingc-
di-GMPsignalingpathwaysisbasedonc-di-GMPlevels,withthesecondmessengerbeing
enzymatically modulated by diguanylate cyclases (DCG), proteins containing a GGDEF
domain, and phosphodiesterases (PDE) containing either an EAL or HD-GYP domain.
Additionally, riboswitches regulate gene expression in response to cyclic di-GMP concen-
trationsinmanybutnotallbacteria.
ThisvolumeoftheMethodsinMolecularBiologyseriesprovidesacollectionofprotocols
for many of the common experimental approaches used in the burgeoning field of c-di-
GMP-dependentsignalingtosynthesize,detect,quantitate,andmodulatethelevelsofc-di-
GMPpresentincells.Additionally,procedurestodetectandevaluatetheinteractionofc-di-
GMP with proteins and bacterial response to varying c-di-GMP levels including virulence,
swarming, and matrix production are included. Additionally, some less common but up-
and-comingapproachesfocusingontheinhibitionofc-di-GMPsignalingareincluded.
This bookisdivided into eightmajorparts,reflectingthebreath oftechniques usedin
the field of c-di-GMP. The chapters are as follows: synthesis of c-di-GMP, detection and
quantitation of c-di-GMP, visualizing c-di-GMP levels using biosensors, indirect detection
ofc-di-GMPlevels,modulationofc-di-GMPlevelsandbacterialresponses,measuringc-di-
GMPmodulatingactivities,c-di-GMPbindingproteins,andtargetingc-di-GMPsignaling.
Themethodschaptersareprecededbyareviewonthediscoveryoftheintracellularsignaling
moleculec-di-GMP.Presentedmethodsarediverseandrangefromthinlayerchromatogra-
phy(TLC)andmassspectrometrytofluorescence-activatedcellsorting(FACS),footprint-
ing,pulldownassays,andisothermaltitrationcalorimetrytomethodsaimingatinhibitingc-
di-GMP-dependentsignalingandvirulencemodels.
All chapters are written in the same format as that used in the Methods in Molecular
Biology™ series. Each chapter opens with a description of the basic theory behind the
method being described. The Materials section lists all the chemicals, reagents, buffers,
and other materials necessary for carrying out the protocol. Since the principal goal of the
book is to provide experimentalists with a full account of the practical steps necessary for
carryingouteachprotocolsuccessfully,theMethodssectioncontainsdetailedstep-by-step
descriptions of every protocol that should result in the successful completion of each
method. The Notes section complements the Methods section by indicating how best to
dealwithanyproblemordifficultythatmightarisewhenusingagiventechnique.Consid-
ering the contribution of c-di-GMP to biofilm formation, with the human pathogen
Pseudomonas aeruginosabeing a paradigm organism for the study ofbiofilm communities,
the book is most detailed for P. aeruginosa but includes also protocols for other model
v
vi Preface
species such as Escherichia coli, Salmonella enterica serovar Typhimurium, Xanthomonas
campestris,andMyxococcusxanthus.
Together,Ihopethatthisvolumewillbeanessentialpartofmanylaboratorylibraries.
However,Ihopethatthisbookismoreoftenonthebenchtopthaninthebookshelfand
inspireresearcherstostepoutoftheircomfortzoneandtrytheirhandsonnewapproaches.
Binghamton,NY,USA KarinSauer
Contents
Preface ..................................................................... v
Contributors................................................................. xi
1 DiscoveryoftheSecondMessengerCyclicdi-GMP......................... 1
UteR¨omlingandMichaelY.Galperin
PART I SYNTHESIS OF C-DI-GMP
2 EnzymaticProductionofc-di-GMPUsingaThermophilicDiguanylate
Cyclase ................................................................ 11
PrabhadeviVenkataramaniandZhao-XunLiang
3 Synthesisof[32P]-c-di-GMPforDiguanylateCyclaseandPhosphodiesterase
ActivityDeterminations.................................................. 23
BarbaraI.Kazmierczak
PART II DETECTION AND QUANTITATION OF C-DI-GMP
4 High-PerformanceLiquidChromatography(HPLC)-BasedDetection
andQuantitationofCellularc-di-GMP.................................... 33
OlgaE.PetrovaandKarinSauer
5 IdentificationandQuantificationofCyclicDi-GuanosineMonophosphate
andItsLinearMetabolitesbyReversed-PhaseLC-MS/MS .................. 45
HeikeBa€hreandVolkhardKaever
6 DetectionofCyclicDinucleotidesbySTING............................... 59
Xiao-XiaDuandXiao-DongSu
7 SpectrophotometricandMassSpectroscopicMethodsfor theQuantification
andKineticEvaluationofInVitroc-di-GMPSynthesis...................... 71
GeoffreyB.SeverinandChristopherM.Waters
PART III VISUALIZING C-DI-GMP LEVELS USING BIOSENSORS
8 GaugingandVisualizingc-di-GMPLevelsinPseudomonasaeruginosa
UsingFluorescence-BasedBiosensors ..................................... 87
MortenRybtke,SongLinChua,JoeyKuokHoongYam,
MichaelGivskov,LiangYang,andTimTolker-Nielsen
9 Cyclicdi-GMP-ResponsiveTranscriptionalReporterBioassays
inPseudomonasaeruginosa............................................... 99
BradleyR.Borlee,GraceI.Borlee,KevinH.Martin,
andYasuhikoIrie
10 LiveFlowCytometryAnalysisofc-di-GMPLevelsinSingle
CellPopulations........................................................ 111
JongchanYeo,XinC.Wang,andMingC.Hammond
vii
viii Contents
PART IV INDIRECT DETECTION OF C-DI-GMP LEVELS
11 ExperimentalDetectionandVisualizationoftheExtracellular
MatrixinMacrocolonyBiofilms .......................................... 133
DiegoO.SerraandRegineHengge
12 CongoRedStainIdentifiesMatrixOverproductionandIsanIndirect
Measurementforc-di-GMPinManySpeciesofBacteria..................... 147
ChristopherJ.JonesandDanielJ.Wozniak
13 TypeIVPili-DependentMotilityasaTooltoDeterminetheActivity
ofc-di-GMPModulatingEnzymesinMyxococcusxanthus.................... 157
DorotaSkotnickaandLotteSøgaard-Andersen
PART V MODULATION OF C-DI-GMP LEVELS AND BACTERIAL RESPONSES
14 UsingLight-ActivatedEnzymesforModulatingIntracellular
c-di-GMPLevelsinBacteria.............................................. 169
Min-HyungRyu,AnastasiaFomicheva,LindseyO’Neal,
GladysAlexandre,andMarkGomelsky
15 Analysisofc-di-GMPLevelsSynthesizedbyaPhotoreceptor
ProteininResponsetoDifferentLightQualities
UsinganInVitroEnzymaticAssay ....................................... 187
VeronikaAngerer,Lars-OliverEssen,andAnnegretWilde
16 ProbingtheRoleofCyclicdi-GMPSignalingSystemsinDisease
UsingChineseRadish................................................... 205
Shi-QiAn,Ji-LiangTang,andJ.MaxwellDow
17 ContributionofCyclicdi-GMPintheControlofTypeIII
andTypeVISecretioninPseudomonasaeruginosa .......................... 213
RonanR.McCarthy,MartinaValentini,andAlainFilloux
18 SemiquantitativeAnalysisoftheRed,Dry,andRoughColony
MorphologyofSalmonellaentericaSerovarTyphimurium
andEscherichiacoliUsingCongoRed..................................... 225
AnnikaCimdinsandRogerSimm
PART VI MEASURING C-DI-GMP MODULATING ACTIVITIES
19 Fluorescent2-Aminopurinec-di-GMPandGpGAnalogs
asPDEProbes ......................................................... 245
JieZhou,ClementOpoku-Temeng,andHermanO.Sintim
20 MeasuringCyclicDiguanylate(c-di-GMP)-SpecificPhosphodiesterase
ActivityUsingtheMANT-c-di-GMPAssay ................................ 263
DoritEli,TrevorE.Randall,HenrikAlmblad,JoeJ.Harrison,
andEhudBanin
21 DeterminingPhosphodiesteraseActivity(RadioactiveAssay)................. 279
BarbaraI.Kazmierczak
22 DeterminingDiguanylateCyclaseActivity(RadioactiveAssay) ............... 285
BarbaraI.Kazmierczak
Contents ix
PART VII C-DI-GMP BINDING PROTEINS
23 Detectionofc-di-GMP-ResponsiveDNABinding.......................... 293
JacobR.ChambersandKarinSauer
24 UseofNonradiochemicalDNAseFootprintingtoAnalyze
c-di-GMPModulationofDNA-BindingProteins........................... 303
ClaudineBaraquetandCarolineS.Harwood
25 DetectionofCyclicdi-GMPBindingProteinsUtilizingaBiotinylated
Cyclicdi-GMPPull-DownAssay ......................................... 317
JacobR.ChambersandKarinSauer
26 ProbingProtein–ProteinInteractionswithGeneticallyEncoded
PhotoactivatableCross-Linkers........................................... 331
RichardB.CooleyandHolgerSondermann
27 Identificationofc-di-AMP-BindingProteinsUsingMagneticBeads .......... 347
JanKampf,JanGundlach,ChristinaHerzberg,KatrinTreffon,
andJ¨orgStu€lke
28 Pull-Downwithac-di-GMP-SpecificCaptureCompoundCoupled
toMassSpectrometryasaPowerfulTooltoIdentifyNovel
EffectorProteins........................................................ 361
Benoıˆt-JosephLaventie,TimoGlatter,andUrsJenal
29 Identificationofc-di-GMP-ResponsiveRiboswitches........................ 377
JohannPeltierandOlgaSoutourina
30 IsothermalTitrationCalorimetrytoDetermineApparentDissociation
Constants(K )andStoichiometryofInteraction(n)ofC-di-GMP
d
BindingProteins........................................................ 403
BrunoY.Matsuyama,PetyaV.Krasteva,andMarcosV.A.S.Navarro
PART VIII TARGETING C-DI-GMP SIGNALING
31 Targetingc-di-GMPSignaling,BiofilmFormation,andBacterial
MotilitywithSmallMolecules............................................ 419
ClementOpoku-TemengandHermanO.Sintim
32 DiscoveringSelectiveDiguanylateCyclaseInhibitors:FromPleD
toDiscriminationoftheActiveSiteofCyclic-di-GMPPhosphodiesterases..... 431
S.Rinaldo,G.Giardina,F.Mantoni,A.Paiardini,AlessioPaone,
andFrancescaCutruzzola`
33 High-ThroughputScreeningforCompoundsthatModulate
theCellularc-di-GMPLevelinBacteria ................................... 455
JulieGroizeleau,JensBoAndersen,MichaelGivskov,JensBerthelsen,
andTimTolker-Nielsen
34 GeneticToolstoStudyc-di-GMP-DependentSignaling
inPseudomonasaeruginosa............................................... 471
LiviaLeoni,SarikaVishnuPawar,andGiordanoRampioni
Index ...................................................................... 481
Contributors
GLADYSALEXANDRE (cid:2) DepartmentofBiochemistry,CellularandMolecularBiology,
TheUniversityofTennessee,Knoxville,TN,USA
HENRIK ALMBLAD (cid:2) DepartmentofBiologicalSciences,UniversityofCalgary,Calgary,AB,
Canada
SHI-QIAN (cid:2) DivisionofMolecularMicrobiology,CollegeofLifeSciences,Universityof
Dundee,Dundee,UK
JENS BOANDERSEN (cid:2) DepartmentofImmunologyandMicrobiology,FacultyofHealthand
MedicalSciences,UniversityofCopenhagen,Copenhagen,Denmark
VERONIKAANGERER (cid:2) InstituteofBiologyIII,Albert-Ludwigs-UniversityFreiburg,Freiburg,
Germany
HEIKEB€aHRE (cid:2) ResearchCoreUnitMetabolomics,InstituteofPharmacology,Hannover
MedicalSchool,Hannover,Germany
EHUDBANIN (cid:2) TheMinaandEverardGoodmanFacultyofLifeSciences,Center for
AdvancedMaterialsandNanotechnology,Bar-IlanUniversity,Ramat-Gan,Israel
CLAUDINEBARAQUET (cid:2) DepartmentofMicrobiology,UniversityofWashington,Seattle,WA,
USA;Universite´ deToulon,MAPIEM,EA4323,LaGarde,France
JENS BERTHELSEN (cid:2) DepartmentofImmunologyandMicrobiology,FacultyofHealthand
MedicalSciences,UniversityofCopenhagen,Copenhagen,Denmark
BRADLEYR.BORLEE (cid:2) DepartmentofMicrobiology,ImmunologyandPathology,Infectious
DiseaseResearchCenter,ColoradoStateUniversity,FortCollins,CO,USA
GRACE I.BORLEE (cid:2) DepartmentofMicrobiology,ImmunologyandPathology,Infectious
DiseaseResearchCenter,ColoradoStateUniversity,FortCollins,CO,USA
JACOBR.CHAMBERS (cid:2) DepartmentofBiologicalSciences,BinghamtonBiofilmResearch
Center,BinghamtonUniversity,Binghamton,NY,USA
SONG LINCHUA (cid:2) SingaporeCenteronEnvironmentalLifeSciencesEngineering,
NanyangTechnologicalUniversity,Singapore,Singapore
ANNIKACIMDINS (cid:2) DepartmentofMicrobiology,TumorandCellBiology,Karolinska
Institutet,Stockholm,Sweden;InstituteofHygiene,UniversityofMu€nster,Mu€nster,
Germany
RICHARDB.COOLEY (cid:2) DepartmentofMolecularMedicine,CollegeofVeterinaryMedicine,
CornellUniversity,Ithaca,NY,USA;DepartmentofBiochemistryandBiophysics,
OregonStateUniversity,Corvallis,OR,USA
FRANCESCACUTRUZZOLA` (cid:2) DepartmentofBiochemicalSciences,IstitutoPasteur
Italia-FondazioneCenciBolognetti,SapienzaUniversityofRome,Rome,Italy
XIAO-XIADU (cid:2) BiodynamicOpticalImagingCenter(BIOPIC),SchoolofLifeSciences,
PekingUniversity,Beijing,China;StateKeyLaboratoryofProteinandPlantGene
Research,SchoolofLifeSciences,PekingUniversity,Beijing,China
DORITELI (cid:2) TheMinaandEverardGoodmanFacultyofLifeSciences,Center for
AdvancedMaterialsandNanotechnology,Bar-IlanUniversity,Ramat-Gan,Israel
LARS-OLIVER ESSEN (cid:2) DepartmentofChemistry,Philipps-UniversityMarburg,Marburg,
Germany
ALAINFILLOUX (cid:2) DepartmentofLifeSciences,MRCCentreforMolecularBacteriology
andInfection,ImperialCollegeLondon,London,UK
xi