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Coverphotocredit: GirouardH.,andTabatabaeiS.N. NitricOxideandCerebrovascularRegulation VitaminsandHormones(2014)96,pp.347–386 AcademicPressisanimprintofElsevier 225WymanStreet,Waltham,MA02451,USA 525BStreet,Suite1800,SanDiego,CA92101-4495,USA 32JamestownRoad,LondonNW17BY,UK TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UK Firstedition2014 Copyright©2014ElsevierInc.Allrightsreserved. Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans, electronicormechanical,includingphotocopying,recording,oranyinformationstorageand retrievalsystem,withoutpermissioninwritingfromthepublisher.Detailsonhowtoseek permission,furtherinformationaboutthePublisher’spermissionspoliciesandour arrangementswithorganizationssuchastheCopyrightClearanceCenterandtheCopyright LicensingAgency,canbefoundatourwebsite:www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightby thePublisher(otherthanasmaybenotedherein). 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THIMANN Newton, Massachusetts University of California Santa Cruz, California JOHN A. LORRAINE IRA G. WOOL University of Edinburgh Edinburgh, Scotland University of Chicago Chicago, Illinois PAUL L. MUNSON EGON DICZFALUSY University of North Carolina Chapel Hill, North Carolina Karolinska Sjukhuset Stockholm, Sweden JOHN GLOVER ROBERT OLSEN University of Liverpool Liverpool, England School of Medicine State University of New York GERALD D. AURBACH at Stony Brook Stony Brook, New York Metabolic Diseases Branch National Institute of DONALD B. MCCORMICK Diabetes and Digestive and Kidney Diseases Department of Biochemistry National Institutes of Health Emory University School of Bethesda, Maryland Medicine, Atlanta, Georgia CONTRIBUTORS AshokAiyar StanleyS.ScottCancerCenter,LouisianaStateUniversity,HealthSciencesCenter,New Orleans,Louisiana,USA AlexisBavencoffe CenterforNeuroscienceandPainResearch,DepartmentofAnesthesiologyand PerioperativeMedicine,TheUniversityofTexasMDAndersonCancerCenter,Houston, Texas,USA KarinC.Calaza ProgramadeNeurocieˆncias,andDepartamentodeNeurobiologia,InstitutodeBiologia, UniversidadeFederalFluminense,Nitero´i,RJ,Brazil PaulaCampello-Costa ProgramadeNeurocieˆncias,andDepartamentodeNeurobiologia,InstitutodeBiologia, UniversidadeFederalFluminense,Nitero´i,RJ,Brazil Shao-RuiChen CenterforNeuroscienceandPainResearch,DepartmentofAnesthesiologyand PerioperativeMedicine,TheUniversityofTexasMDAndersonCancerCenter,Houston, Texas,USA AngelaCheung DivisionofDevelopmentalNeurobiology,MRCNationalInstituteforMedicalResearch, MillHill,London,UnitedKingdom MarceloCossenza ProgramadeNeurocieˆncias,InstitutodeBiologia,Nitero´i,RJ,andDepartamentode FisiologiaeFarmacologia,InstitutoBiome´dico,UniversidadeFederalFluminense, RiodeJaneiro,Brazil IvanC.L.Domith ProgramadeNeurocieˆncias,InstitutodeBiologia,UniversidadeFederalFluminense, Nitero´i,RJ,Brazil Tha´ısaG.Encarnac¸a˜o ProgramadeNeurocieˆncias,InstitutodeBiologia,UniversidadeFederalFluminense, Nitero´i,RJ,Brazil DavidA.Geller DepartmentofSurgery,UniversityofPittsburgh,Pittsburgh,Pennsylvania,USA He´le`neGirouard DepartmentofPharmacology,FacultyofMedicine,Universite´deMontre´al,andResearch CenteroftheInstitutUniversitairedeGe´riatriedeMontre´al,Montreal,Quebec,Canada xiii xiv Contributors LuisF.H.Gladulich ProgramadeNeurocieˆncias,InstitutodeBiologia,UniversidadeFederalFluminense, Nitero´i,RJ,Brazil WilliamP.Gray InstituteofPsychologicalMedicineandClinicalNeurosciences,CardiffUniversity,Cardiff, UnitedKingdom ZhongGuo DepartmentofSurgery,UniversityofPittsburgh,Pittsburgh,Pennsylvania,USA BradfordG.Hill DiabetesandObesityCenter,InstituteofMolecularCardiology;DepartmentofPhysiology andBiophysics,andDepartmentofBiochemistryandMolecularBiology,Universityof LouisvilleSchoolofMedicine,Louisville,Kentucky,USA MichaelA.Hough SchoolofBiologicalSciences,UniversityofEssex,Colchester,UnitedKingdom YaoHu InstituteforStemCellsandNeuralRegeneration,SchoolofPharmacy,NanjingMedical University,Nanjing,China H.S.JeffreyMan InstituteofMedicalScience;LiKaShingKnowledgeInstitute,St.Michael’sHospital,and DivisionsofRespirologyandCriticalCareMedicine,DepartmentofMedicine,University ofToronto,Toronto,Ontario,Canada JishaJoshua DepartmentofMedicine,UniversityofCalifornia,SanDiego,California,USA HemaKalyanaraman DepartmentofMedicine,UniversityofCalifornia,SanDiego,California,USA SangwonF.Kim DepartmentofPsychiatryandPharmacology,CenterforNeurobiologyandBehavior,The PerelmanSchoolofMedicineatUniversityofPennsylvania,Philadelphia,Pennsylvania, USA PeterKruzliak DepartmentofCardiovascularDiseases,InternationalClinicalResearchCenter,St.Anne’s UniversityHospital,Brno,CzechRepublic NishaMarathe DepartmentofMedicine,UniversityofCalifornia,SanDiego,California,USA PhilipA.Marsden InstituteofMedicalScience;LiKaShingKnowledgeInstitute,St.Michael’sHospital,and DivisionofNephrology,DepartmentofMedicine,UniversityofToronto,Toronto, Ontario,Canada JunkoMaruyama DepartmentofAnesthesiologyandCriticalCareMedicine,MieUniversitySchoolof Medicine,andDepartmentofClinicalEngineering,SuzukaUniversityofMedicalScience, Mie,Japan Contributors xv KazuoMaruyama DepartmentofAnesthesiologyandCriticalCareMedicine,MieUniversitySchoolof Medicine,andDepartmentofClinicalEngineering,SuzukaUniversityofMedicalScience, Mie,Japan HenriqueR.Mendonc¸a ProgramadeNeurocieˆncias,InstitutodeBiologia,UniversidadeFederalFluminense, Nitero´i,RJ,Brazil RobertoPaes-de-Carvalho ProgramadeNeurocieˆncias,andDepartamentodeNeurobiologia,InstitutodeBiologia, UniversidadeFederalFluminense,Nitero´i,RJ,Brazil Hui-LinPan CenterforNeuroscienceandPainResearch,DepartmentofAnesthesiologyand PerioperativeMedicine,TheUniversityofTexasMDAndersonCancerCenter,Houston, Texas,USA RenateB.Pilz DepartmentofMedicine,UniversityofCalifornia,SanDiego,California,USA CamilaC.Portugal ProgramadeNeurocieˆncias,InstitutodeBiologia,UniversidadeFederalFluminense, Nitero´i,RJ,Brazil BrianE.Sansbury DiabetesandObesityCenter,InstituteofMolecularCardiology,andDepartmentof PhysiologyandBiophysics,Louisville,Kentucky,USA GarySilkstone SchoolofBiologicalSciences,UniversityofEssex,Colchester,UnitedKingdom RenatoSocodato ProgramadeNeurocieˆncias,InstitutodeBiologia,UniversidadeFederalFluminense, Nitero´i,RJ,Brazil SeyedNasrollahTabatabaei DepartmentofComputerandSoftwareEngineeringandInstituteofBiomedical (cid:1) Engineering,EcolePolytechniquedeMontre´al DavidTate StanleyS.ScottCancerCenter,LouisianaStateUniversity,HealthSciencesCenter,New Orleans,Louisiana,USA DouglasD.Thomas DepartmentofMedicinalChemistryandPharmacognosy,UniversityofIllinoisatChicago, Chicago,Illinois,USA AlbertK.Y.Tsui LiKaShingKnowledgeInstitute,andDepartmentofAnesthesia,St.Michael’sHospital, Toronto,Ontario,Canada LauraB.Valdez InstituteofBiochemistryandMolecularMedicine(IBIMOL),PhysicalChemistryDivision, SchoolofPharmacyandBiochemistry,UniversityofBuenosAires,BuenosAires,Argentina xvi Contributors DivyaVasudevan DepartmentofMedicinalChemistryandPharmacognosy,UniversityofIllinoisatChicago, Chicago,Illinois,USA CeciliaVecoli InstituteofClinicalPhysiology-CNR,Pisa,Italy MichaelT.Wilson SchoolofBiologicalSciences,UniversityofEssex,Colchester,UnitedKingdom JonathanWorrall SchoolofBiologicalSciences,UniversityofEssex,Colchester,UnitedKingdom TamaraZaobornyj InstituteofBiochemistryandMolecularMedicine(IBIMOL),PhysicalChemistryDivision, SchoolofPharmacyandBiochemistry,UniversityofBuenosAires,BuenosAires,Argentina ArnoldH.Zea StanleyS.ScottCancerCenter,LouisianaStateUniversity,HealthSciencesCenter,New Orleans,Louisiana,USA Dong-YaZhu InstituteforStemCellsandNeuralRegeneration,andDepartmentofPharmacology,School ofPharmacy,NanjingMedicalUniversity,Nanjing,China PREFACE Nitricoxide(nitrogenmonoxide,NO),agaseousmolecule,isderivedfrom the amino acid, L-arginine, in the human body. Its discovery was a great surprise because other hormones and regulators in the body are made up ofproteins,lipid-derivedcompounds,andothermolecules,noneofwhich are gaseous. NO affects a number of enzyme systems and binds to heme, a cofactorinsomeimportantenzymes.Inmanyways,NOactsasahormone and regulates many processes. Its activities are generally beneficial. For example, it is a powerful generator of vasodilation by suppressing vascular smooth muscle contraction. Its action is rapid as it remains in the blood for only seconds. In other activities, NO inhibits platelet aggregation and the adhesion of leukocytes to endothelia. Poorly functioning pathways involvingNOarehallmarksinpatientswithvariousdiseases,suchasdiabe- tes,atherosclerosis,andhypertension.Consequently,nitricoxidebecomesa substanceofinterestintherapeuticapplications.Manyofthepropertiesand actions of this new regulator, nitric oxide, are reviewed in this volume. Reviews in this book have been ordered by first introducing the basic aspects of nitric oxide followed by chapters that involve clinical concepts. Accordingly,thefirstchapterisonthe“Regulationofnociceptivetransduc- tion and transmission by nitric oxide” by A. Bavencoffe, S.-R. Chen, and H.-L. Pan. The next offering is by Z. Guo and D.A. Geller entitled “microRNA and human inducible nitric oxide synthase.” “Heart mitochondrial nitric oxide synthase: a strategic enzyme in the regulation of cellular bioenergetics” is authored by T. Zaobornyj and L.B. Valdez. W.P. Gray and A. Cheung review “Nitric oxide regulation of adult neurogenesis.”“Nitricoxideinthenervoussystem:biochemical,develop- mental, and neurobiological aspects” is the work of M. Cossenza, R. Socodato, C.C. Portugal, I.C.L. Domith, L.F.H. Gladulich, T.G. Encarnac¸a˜o, K.C. Kalaza, H.R. Mendonc¸a, P. Campello-Costa, and R. Paes-de-Carvalho. Y. Hu and D.-Y. Zhu report on “Hippocampus and nitric oxide.” “Nitric oxide and hypoxia signaling” is a review by H.S.J. Man, A.K.Y. Tsui, and P.A. Marsden. M.A. Hough, G. Silkstone, J. Worrall, and M.T. Wilson discuss “NO binding to the proapoptotic cytochrome c–cardiolipin complex.” S.F. Kim writes on “The nitric oxide-mediated regulation of prostaglandin signaling in medicine.” xvii xviii Preface “Nitricoxideasamediatorofestrogeneffectsinosteocytes”isthetopicof J. Joshua, H. Kalyanaraman, N. Marathe, and R.B. Pilz. In aspects related to disease conditions, contributions begin with “Insights into the diverse effects of nitric oxide on tumor biology” by D. Vasudevan and D.D. Thomas. A.H. Zea, A. Aiyar, and D. Tate review “Dual effect of interferon (IFNγ)-induced nitric oxide on tumorigenesis and intracellular bacteria.” Next, B.E. Sansbury and B.G. Hill cover the “Anti-obesogenic role of endothelial nitric oxide synthase.” H. Girouard and S.N. Tabatabaei report on “Nitric oxide and cerebrovascular regulation.” Then, C.Vecoli reports on “Endothelialnitric oxidesynthase genepolymorphismsincardiovasculardisease.”The“Roleofnitricoxidein pathophysiologyandtreatmentofpulmonaryhypertension”byP.Kruzliak, J. Maruyama, and K. Maruyama is the final chapter. The cover illustration is Fig. 14.2 of Chapter 14. HeleneKabesandMaryAnnZimmermanofElsevier,Oxford,UKwere instrumental in the processing of these chapters. GERALD LITWACK North Hollywood, California May 8, 2014 CHAPTER ONE Regulation of Nociceptive Transduction and Transmission by Nitric Oxide Alexis Bavencoffe, Shao-Rui Chen, Hui-Lin Pan1 CenterforNeuroscienceandPainResearch,DepartmentofAnesthesiologyandPerioperativeMedicine, TheUniversityofTexasMDAndersonCancerCenter,Houston,Texas,USA 1Correspondingauthor:e-mailaddress:[email protected] Contents 1. Introduction 2 2. RoleofNOinNociceptiveTransductionatthePeriphery 3 3. DiverseEffectsofNOonIonChannelsExpressedonPrimarySensoryNeurons 5 3.1 Acid-sensingionchannels 5 3.2 Transientreceptorpotentialchannels 5 3.3 K channels 7 ATP 4. RoleofNOinRegulatingNociceptiveTransmissionattheSpinalCordLevel 7 5. NOReducesExcitatory,ButPotentiatesInhibitory,SynapticTransmission inSpinalCords 9 5.1 Glutamatergicinputfromprimaryafferentnerves 10 5.2 Voltage-activatedcalciumchannelsinsensoryneurons 11 5.3 SynapticNMDAreceptors 11 5.4 Synapticreleaseofglycine 11 6. ConclusionsandFutureDirections 12 Acknowledgments 14 References 14 Abstract Thepotentialinvolvementofnitricoxide(NO),adiffusiblegaseoussignalingmessenger, innociceptivetransductionandtransmissionhasbeenextensivelyinvestigated.How- ever, there is no consistent and convincing evidence supporting the pronociceptive action of NO at the physiological concentration, and the discrepancies are possibly duetothenonspecificityofnitricoxidesynthaseinhibitorsanddifferentconcentrations of NO donors used in various studies. At the spinal cord level, NO predominantly reducessynaptictransmissionbyinhibitingtheactivityofNMDAreceptorsandgluta- mate release from primary afferent terminals through S-nitrosylation of voltage- activatedcalciumchannels.NOalsopromotessynapticglycinereleasefrominhibitory VitaminsandHormones,Volume96 #2014ElsevierInc. 1 ISSN0083-6729 Allrightsreserved. http://dx.doi.org/10.1016/B978-0-12-800254-4.00001-5 2 AlexisBavencoffeetal. interneuronsthroughthecyclicguanosinemonophosphate/proteinkinaseGsignaling pathway.Thus,NOprobablyfunctionsasanegativefeedbackregulatortoreducenoci- ceptivetransmissioninthespinaldorsalhornduringpainfulconditions. 1. INTRODUCTION Painreceptors,alsocallednociceptors,areagroupofsensoryneurons with specialized nerve endings widely distributed in the skin, deep tissues (includingthemusclesandjoints),andmostofvisceralorgans.Theyrespond to tissue injury or potentially damaging stimuli by sending nerve signals to thespinalcordandbraintobegintheprocessofpainsensation.Nociceptors areequippedwithspecificmolecularsensors,whichdetectextremeheator cold and certain harmful chemicals. Mechanical nociceptors can also respond to tissue-damaging stimuli, such as pinching the skin or over- stretchingthemuscles.Activationofnociceptorsgeneratesactionpotentials, which are propagated along the afferent nerve axons, especially unmyelin- ated C-fibers and thinly myelinated Aδ-fibers. At the spinal cord level, the nociceptive nerve terminals release excitatory neurotransmitters to activate theirrespectivepostsynapticreceptorsonsecond-orderneurons.Inthespi- naldorsalhorn,bothexcitatoryandinhibitoryinterneuronscanaugmentor attenuate nociceptive transmission (Cervero & Iggo, 1980; Zhou, Zhang, Chen, & Pan, 2007, 2008). The nociceptive signal, encoding the quality, location, and intensity of the noxious stimuli, is then conveyed via the ascending pathway to reach various brain regions to elicit pain sensation. Physiological pain responses normally protect us from tissue damage by quickly alerting us to impending injury. Unlike acute physiological pain, chronic pathological pain, including neuropathic and inflammatory pain, isoftenassociatedwithincreasedactivityandresponsesofspinaldorsalhorn neurons, termed central sensitization (Woolf & Thompson, 1991; Xu, Dalsgaard, & Wiesenfeld-Hallin, 1992). This phenomenon is the cellular basis for hyperalgesia (increased pain response to a noxious stimulus) and allodynia (painful sensation in response to a nonnoxious stimulus). Nitricoxide(NO)isamembrane-permeablegaseoussecondmessenger involvedinsignaltransduction.ThephysiologicalfunctionofNOhasbeen showninalargevarietyofcelltypesandtissues,includingtheimmunesys- tem, blood vessels, endothelial cells, and neurons. NO is produced from L-argininebythreemajorisoformsofnitricoxidesynthase(NOS):neuronal
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