Hydrogen sulfide in redox biology. Volume 554, Part A

321 Pages·2015·13.46 MB·English

by  Abou-Hamdan

METHODS IN ENZYMOLOGY
Editors-in-Chief
JOHN N. ABELSON and MELVIN I. SIMON
Division of Biology
California Institute of Technology
Pasadena, California
ANNA MARIE PYLE
Departments of Molecular, Cellular and Developmental
Biology and Department of Chemistry Investigator
Howard Hughes Medical Institute
Yale University
Founding Editors
SIDNEY P. COLOWICK and NATHAN O. KAPLAN
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CONTRIBUTORS
AbbasAbou-Hamdan
InsermU1016;CNRSUM8104,andUniversite´ ParisDescartesUMR-S1016,Institut
Cochin,Paris,France
MireilleAndriamihaja
INRA-CRNH-IdF-AgroParisTech,UMR914NutritionPhysiologyandIngestive
Behavior,Paris,France
RumaBanerjee
DepartmentofBiologicalChemistry,UniversityofMichiganMedicalSchool,AnnArbor,
Michigan,USA
Jin-SongBian
DepartmentofPharmacology,YongLooLinSchoolofMedicine,NationalUniversityof
Singapore,Singapore
Franc¸oisBlachier
INRA-CRNH-IdF-AgroParisTech,UMR914NutritionPhysiologyandIngestive
Behavior,Paris,France
Fre´de´ricBouillaud
InsermU1016;CNRSUM8104,andUniversite´ ParisDescartesUMR-S1016,Institut
Cochin,Paris,France
ChristopherJ.Chang
DepartmentofChemistry;DepartmentofMolecularandCellBiology,Universityof
California,Berkeley,California,andHowardHughesMedicalInstitute,ChevyChase,
Maryland,USA
TauraiChiku
DepartmentofBiologicalChemistry,UniversityofMichiganMedicalSchool,AnnArbor,
Michigan,USA
BrianW.Dymock
DepartmentofPharmacy,NationalUniversityofSingapore,Singapore
HalaGuedouari-Bounihi
InsermU1016;CNRSUM8104,andUniversite´ ParisDescartesUMR-S1016,Institut
Cochin,Paris,France
TakaakiIto
DepartmentofPathologyandExperimentalMedicine,GraduateSchoolofMedicalScience,
KumamotoUniversity,Kumamoto,Japan
MichaelR.Jackson
DepartmentofBiochemistryandMolecularBiology,CollegeofMedicine,Drexel
University,Philadelphia,Pennsylvania,USA
xi
xii Contributors
MarilynSchumanJorns
DepartmentofBiochemistryandMolecularBiology,CollegeofMedicine,Drexel
University,Philadelphia,Pennsylvania,USA
OmerKabil
DepartmentofBiologicalChemistry,UniversityofMichiganMedicalSchool,AnnArbor,
Michigan,USA
ChristopherG.Kevil
DepartmentofPathology,LouisianaStateUniversityHealthSciencesCenter–Shreveport,
Shreveport,Louisiana,USA
GopiK.Kolluru
DepartmentofPathology,LouisianaStateUniversityHealthSciencesCenter–Shreveport,
Shreveport,Louisiana,USA
Ve´roniqueLenoir
InsermU1016;CNRSUM8104,andUniversite´ ParisDescartesUMR-S1016,Institut
Cochin,Paris,France
Zhong-GuangLi
SchoolofLifeSciences;EngineeringResearchCenterofSustainableDevelopmentand
UtilizationofBiomassEnergy,MinistryofEducation;KeyLaboratoryofBiomassEnergy
andEnvironmentalBiotechnology,YunnanNormalUniversity,Kunming,Yunnan
Province,PRChina
MarouaneLibiad
DepartmentofBiologicalChemistry,UniversityofMichiganMedicalSchool,AnnArbor,
Michigan,USA
VivianS.Lin
DepartmentofChemistry,UniversityofCalifornia,Berkeley,California,USA
AlexanderR.Lippert
DepartmentofChemistry,andCenterforDrugDiscovery,Design,andDelivery(CD4),
SouthernMethodistUniversity,Dallas,Texas,USA
ScottL.Melideo
DepartmentofBiochemistryandMolecularBiology,CollegeofMedicine,Drexel
University,Philadelphia,Pennsylvania,USA
PhilipK.Moore
NeurobiologyProgram,LifeScienceInstituteandDepartmentofPharmacology,National
UniversityofSingapore,Singapore
NicoleMotl
DepartmentofBiologicalChemistry,UniversityofMichiganMedicalSchool,AnnArbor,
Michigan,USA
NoriyukiNagahara
IsotopeResearchCenter,NipponMedicalSchool,Tokyo,Japan
MasatoshiNagano
DepartmentofPharmacology,NipponMedicalSchool,Tokyo,Japan
Contributors xiii
Pe´terNagy
DepartmentofMolecularImmunologyandToxicology,NationalInstituteofOncology,
Budapest,Hungary
Chung-MinPark
DepartmentofChemistry,WashingtonStateUniversity,Pullman,Washington,USA
BoPeng
DepartmentofChemistry,WashingtonStateUniversity,Pullman,Washington,USA
MichaelD.Pluth
DepartmentofChemistryandBiochemistry,InstituteofMolecularBiology,Materials
ScienceInstitute,UniversityofOregon,Eugene,Oregon,USA
PeterRose
UniversityofLincoln,Lincoln,Lincolnshire,UnitedKingdom
XingguiShen
DepartmentofPathology,LouisianaStateUniversityHealthSciencesCenter–Shreveport,
Shreveport,Louisiana,USA
T.SpencerBailey
DepartmentofChemistryandBiochemistry,InstituteofMolecularBiology,Materials
ScienceInstitute,UniversityofOregon,Eugene,Oregon,USA
HidenoriSuzuki
DepartmentofPharmacology,NipponMedicalSchool,Tokyo,Japan
VictorVitvitsky
DepartmentofBiologicalChemistry,UniversityofMichiganMedicalSchool,AnnArbor,
Michigan,USA
MingXian
DepartmentofChemistry,WashingtonStateUniversity,Pullman,Washington,USA
XueXue
DepartmentofPharmacology,YongLooLinSchoolofMedicine,NationalUniversityof
Singapore,Singapore
PramodK.Yadav
DepartmentofBiologicalChemistry,UniversityofMichiganMedicalSchool,AnnArbor,
Michigan,USA
ShuaiYuan
DepartmentofPathology,LouisianaStateUniversityHealthSciencesCenter–Shreveport,
Shreveport,Louisiana,USA
PREFACE
Hydrogensulfideisviewedasthethirdgasotransmmitter,gaseoussignaling
molecule, together with nitric oxide and carbon monoxide. The cellular
sources of hydrogen sulfide involve enzymes of the trans-sulfuration path-
wayCBS(cystathionineβ-synthase),CSE(cystathioineγ-lyase),and3MST
(3-mercaptopyruvatesulfur-transferase).Storagesofhydrogensulfideoccur
inmitochondria(iron–sulfurclustersofenzymes)andcytosol(boundsulfane
sulfur). Of course, the release of hydrogen sulfide from these storages is
tightly regulated by several pathophysiological processes.
In addition to the myriad of effects arising from hydrogen sulfide as a
signalingmolecule,italsoprotectsagainstoxidativestressandglutamatetox-
icity,inhibitsthereleaseofinsulin,preservesmitochondrialfunction,andisa
modulatorofinflammatoryresponses.Thesepleiotropiceffectsofhydrogen
sulfidehavebeenthesubjectofnumerousinvestigationsinthelastyearsand
are largely accounted for by as its role as a gaseous signaling molecule.
Hydrogen sulfide may act alone or in conjunction with other gas-
otransmitters and, in doing so, it regulates a number of physiological pro-
cessesandisinvolvedinsomestagesofthepathogenesisofseveraldiseases.
These volumes of Methods in Enzymology were designed as a compen-
diumforhydrogensulfidedetectionmethods,thepharmacologicalactivity
ofhydrogensulfidedonors,theredoxbiochemistryofhydrogensulfideand
itsmetabolisminmammaliantissues,themechanismsinherentinhydrogen
sulfidecellsignalingandtranscriptionalpathways,andcellsignalinginspe-
cificsystems,suchascardiovascularandnervoussystemaswellasitsfunction
in inflammatory responses. Three chapters are also devoted to hydrogen
sulfideinplantsandanewcomer,molecularhydrogen,itsfunctionasanovel
antioxidant.
In bringing these volumes of Methods in Enzymology to fruition, credit
mustbegiventotheexpertsinvariousaspectsofhydrogensulfideresearch,
whose thorough and innovative work is the basis of these Methods in
Enzymology volumes. We hope that these volumes will be of help to both
new and established investigators in the field.
ENRIQUE CADENAS
LESTER PACKER
xv
CHAPTER ONE
Mechanistic Chemical Perspective
of Hydrogen Sulfide Signaling
Péter Nagy1
DepartmentofMolecularImmunologyandToxicology,NationalInstituteofOncology,Budapest,Hungary
1Correspondingauthor:e-mailaddress:[email protected]
Contents
1. Introduction 5
2. BioavailabilityofSulfide—TheSignal 5
2.1 Endogenoussulfideproduction 6
2.2 Sulfidecatabolism 8
2.3 Endogenoussulfidebuffers 9
3. InorganicPolysulfides 9
3.1 Biologicalrelevance 9
3.2 Speciationandredoxcapacityofpolysulfides 10
3.3 Polysulfideformationbysulfideoxidation 11
3.4 Stabilityofpolysulfides 12
4. SulfideSignalingViaProteinSulfhydration 13
4.1 Mechanismsofpersulfideformation 14
5. SulfideSignalingviaSulfide–HemeproteinInteractions 18
5.1 Sulfidemediateshemeproteinfunctions 19
5.2 Hemeproteinsgeneratesulfideoxidationproducts 21
5.3 Antioxidantpropertiesofsulfideviareductionofmetal
centerswithhigheroxidationstates 22
6. Conclusions 23
Acknowledgments 24
References 24
Abstract
Hydrogensulfideisnowawell-appreciatedmasterregulatorinadiversearrayofphys-
iologicalprocesses.However,asaconsequenceoftherapidgrowthofthearea,sulfide
biologysuffersfromanincreasingnumberofcontroversialobservationsandinterpre-
tations. A better understanding of the underlying molecular pathways of sulfide's
actions is key to reconcile controversial issues, which calls for rigorous chemical/
biochemicalinvestigations.
Proteinsulfhydrationandcoordination/redoxchemicalinteractionsofsulfidewith
hemeproteinsarethetwomostextensivelystudiedpathwaysinsulfidebiochemistry.
These pathways are important mediators of protein functions, generate bioactive
MethodsinEnzymology,Volume554 #2015ElsevierInc. 3
ISSN0076-6879 Allrightsreserved.
http://dx.doi.org/10.1016/bs.mie.2014.11.036
4 PéterNagy
sulfidemetabolites,contributetosulfidestorage/traffickingandcarryantioxidantfunc-
tions. In addition, inorganic polysulfides, which are oxidative sulfide metabolites, are
increasinglyrecognizedasimportantplayersinsulfidebiology.
Thischapterprovidesanoverviewofourmechanisticperspectiveonthereactions
thatgovern(i)sulfide'sbioavailability(includingthedelicateenzymemachineriesthat
orchestrate sulfide production and consumption and the roles of the large sulfide-
storingpoolsasbiologicalbuffers),(ii)biologicalsignificanceandmechanismsofper-
sulfide formation (including the reduction of disulfides, condensation with sulfenic
acids, oxidation of thiols with polysulfides and radical-mediated pathways),
(iii)coordinationandredoxchemicalinteractionsofsulfidewithhemeproteins(includ-
ing cytochrome c oxidase, hemoglobins, myoglobins and peroxidases), and (iv) the
chemistryofpolysulfides.
ABBREVIATIONS
3MST 3-mercaptopyruvatesulfurtransferase
AAT aspartate/cysteineaminotransferase
CBS cystathionine-β-synthase
CcO cytochromeCoxidase
CSE cystathionine-γ-lyase
CySOH Cyssulfenicacids
CySSHandGSSH,respectively Cys-andGSH-persulfides
DTNB 5,50-dithiobis-(2-nitrobenzoicacid)
ER endoplasmicreticulum
ERK1/2 extracellularsignal-regulatedkinases½
Ero1 ERoxidoreductin
Erv1 essentialforrespirationandvegetativegrowthsulfhydryloxidase
GAPDH glyceraldehyde-3-phosphatedehydrogenase
GOR glutathioneoxido-reductase
Hb Hemoglobin
HSSH(cid:2)(cid:129) disulfideanionradicalspecies
Keap1 Kelch-likeECH-associatedprotein1
LPO lactoperoxidase
Mb myoglobin
MEK1 mitogen-activatedproteinkinasekinase
MPO myeloperoxidase
NfκB nuclearfactorkappa-light-chain-enhancerofactivatedBcells
Nrf2 nuclearfactor(erythroid-derived2)-like2
PARP-1 poly[ADP-ribose]polymerase1
PDI proteindisulfideisomerase
PLP pyridoxalphosphate
PTEN phosphataseandtensinhomolog
PTP1B protein-tyrosinephosphatase1B
roGFP reduction–oxidationsensitivegreenfluorescentprotein
ROS reactiveoxygenspecies
RPS3 ribosomalproteinS3
SAM S-adenosylmethionine
MechanisticChemistryofSulfideSignaling 5
SDO sulfidedioxigenase
SO sulfiteoxidase
SQR sulfidequinonereductase
SUMO smallubiquitin-likemodifier
TNB 5-thio-2-nitrobenzoicacid
TPO thyroidperoxidase
Trx thioredoxin
TST thiosulfate:glutathionesulfurtransferase
1. INTRODUCTION
Sulfide biology has expanded very rapidly in the past decade with a
great number of groundbreaking fundamental discoveries (see, e.g.,
Abe & Kimura, 1996; Blackstone, Morrison, & Roth, 2005; Coletta
et al., 2012; Elrod et al., 2007; Flannigan et al., 2014; Mustafa et al.,
2009; Papapetropoulos et al., 2009; Suzuki et al., 2011; Szabo et al.,
2013;Yangetal.,2008).However,thefieldsuffersfromasideeffectcom-
montomanyextensivelygrowingareas,thatofgeneratingalargenumberof
controversial reports. Better understanding of the underlying molecular
mechanismsofsulfideactions isafundamental requirementfor reconciling
these controversial physiological observations. Therefore, this review is
intendedtoprovideourmechanisticchemicalperspectiveonwhatarecur-
rently considered to be the most important reactions in sulfide biology.
2. BIOAVAILABILITY OF SULFIDE—THE SIGNAL
In considering the mechanistic details of sulfide signaling, the first
obvious parameter to address is the physiological concentration of sulfide,
i.e.,thesignal.Moreover,indynamic,livingsystems,itisratherthechange
in sulfide concentration over time that triggers the cascade of biochemical
reactions that constitute the signaling process.
Sulfide concentrations can change: (i) as a result of physiological
or pathophysiological events (for example, in some cancer cells the
sulfide-producing enzymes, cystathionine-β-synthase (CBS), and/or
cystathionine-γ-lyase (CSE) are overexpressed and could increase sulfide
levels,butininflammationoratsitesofoxidativestress,sulfidelevelscould
besignificantlydiminished),(ii)duetoadministrationofauthenticsulfideor
slow releasing sulfide donor molecules, or (iii) simply as a result of normal
cellularfunctions.Thelattercanbedemonstratedbythefactthatincellular
6 PéterNagy
systems metabolic pathways work in parallel to strictly govern free sulfide
levels,andasmallperturbationofsulfide-producingorconsumingreactions
can have a profound effect on steady-state concentrations (Vitvitsky,
Kabil, & Banerjee, 2012).
2.1. Endogenous sulfide production
Endogenous sulfide production via cysteine metabolism is catalyzed
by at least three different enzymatic systems, the main ones being the
two pyridoxal phosphate (PLP) dependent CBS and CSE enzymes and
the cooperative actions of aspartate/cysteine aminotransferase (AAT) and
3-mercaptopyruvate sulfurtransferase (3MST) (reviewed recently in Kabil &
Banerjee, 2014; Nagahara, 2013). Although these enzymes all use cysteine
as their biological substrate, their individual enzyme kinetic properties are
very different. Differences include the involvement of (i) a variety of
co-substrates,(ii)parallelenzymaticactivities,and(iii)mechanismsofinhi-
bition/potentiation (Fig. 1).
Therefore,thedominantcysteinemetabolism-mediatedsulfide-producing
pathwayinacertainbiologicalsituationdependsnotonlyontherelativeCSE:
CBS:AAT/3MSTconcentrationsonsite,butalsoonmanyothercomponents
including thebioavailabilityof cysteine, homocysteine, α-ketoglutarate, and
other enzyme activity modulating factors (Chiku et al., 2009; Yadav,
Yamada,Chiku,Koutmos,&Banerjee,2013).Theprimarysulfide-producing
reactionscatalyzedbytheseenzymesarealsoverydifferentchemically:CSEand
CBScatalyzeα,β-eliminationandβ-replacementreactionsofcysteine,respec-
tively, while 3MST produces sulfide via reductive elimination from a pref-
ormedcysteine-persulfideintermediatespecies(seeFig.1).
Twoadditional mechanismshave thepotential to produce sulfide indi-
rectly, from Cys- and GSH-persulfides (CySSH and GSSH, respectively).
TheseareCSE(Yamanishi&Tuboi,1981)andCBS(Idaetal.,2014)cat-
alyzed beta-elimination from cystine and subsequent transsulfuration
betweenCySSHandGSH.Notethatthesepathwaysexcludethedirectpar-
ticipationofsulfideinthepersulfideformationprocess,whichisanimpor-
tant difference from sulfide-mediated persulfide generation reactions (see
later). Based on the measured K and k values, Ida et al. proposed that
M cat
under biologically relevant Cys:CySSCy ratios, CySSCy could be the pre-
ferredsubstrateforCSEandCBS.Hence,thesereactionscouldprovidethe
majority of the large amounts (tens to hundreds of μM-s) of persulfides
(mostly as GSSH) that were detected in cellular systems (Ida et al., 2014).