Stress Resilience: Molecular and Behavioral Aspects PDF
Preview Stress Resilience: Molecular and Behavioral Aspects
STRESS RESILIENCE MOLECULAR AND BEHAVIORAL ASPECTS Edited by A C LON HEN AcademicPress isanimprintofElsevier 125London Wall,London EC2Y5AS,UnitedKingdom 525BStreet,Suite1650,SanDiego,CA92101,UnitedStates 50HampshireStreet,5thFloor, Cambridge,MA02139,UnitedStates TheBoulevard,Langford Lane,Kidlington,OxfordOX5 1GB,UnitedKingdom Copyright©2020ElsevierInc.Allrights reserved. Nopart ofthispublicationmay bereproduced ortransmittedinanyformor byanymeans, electronicor mechanical, includingphotocopying, recording,oranyinformation storageandretrieval system,without permissioninwritingfrom thepublisher.Details onhowtoseekpermission, further informationaboutthe Publisher’spermissions policies andourarrangements withorganizations suchastheCopyrightClearance CenterandtheCopyrightLicensingAgency,canbefoundatourwebsite:www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontained initareprotected undercopyrightbythePublisher (otherthanasmaybenotedherein). 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LibraryofCongressCataloging-in-Publication Data Acatalogrecordforthisbookis availablefromtheLibrary ofCongress BritishLibraryCataloguing-in-Publication Data Acataloguerecord forthisbook isavailablefromtheBritish Library ISBN:978-0-12-813983-7 Forinformation onallAcademic Presspublications visitourwebsite at https://www.elsevier.com/books-and-journals Publisher:NikkiLevy AcquisitionEditor: JoslynChaiprasert-Paguio EditorialProjectManager:KristiAnderson ProductionProjectManager:Prem KumarKaliamoorthi CoverDesigner: Mark Rogers TypesetbyTNQTechnologies Coverdesignby:TaliWiesel,GraphicDesigner,Design, Photography&PrintingBranch,Research Services Division,Weizmann InstituteofScience. This book is dedicated in loving memory of Wylie W. Vale, a founder of mechanistic stress research andtowhomIamforeverindebtedforhisendlessinspirationandencouragement. “Resilienceiscriticalinallthings.Gritandzestarequalitiesmostpredictiveofsuccess.” Wylie W. Vale (1941e2012) v Contributors ElisabethB.Binder DepartmentofTranslational MatthewCranshaw UniversityofMiami,Miller Research in Psychiatry, Max Planck Institute of SchoolofMedicine,Miami,FL,UnitedStates Psychiatry, Munich, Germany; Department of John F. Cryan Department of Anatomy and Psychiatry and Behavioral Sciences and Neuroscience, University College Cork, Cork, Department of Psychology, Emory University Ireland; APCMicrobiomeInstitute,University SchoolofMedicine,Atlanta,GA,UnitedStates CollegeCork,Cork,Ireland Tracy L. Bale Department of Pharmacology, E. Ron de Kloet Department of Endocrinology, University of Maryland School of Medicine, LeidenUniversityMedicalCenter,Leiden,The Baltimore, MD, United States; Center for Netherlands Epigenetic Research inChild Health andBrain Jan M. Deussing Department of Stress Neuro- Development, University of Maryland School biology and Behavioral Neurogenetics, Max ofMedicine,Baltimore,MD,UnitedStates PlanckInstituteofPsychiatry,Munich,Germany Tallie Z. Baram Department of Anatomy/ Olivia Engmann Laboratory of Neuro- Neurobiology, University of California-Irvine, epigenetics, Brain Research Institute, Medical Irvine, CA, United States; Department of Pe- facultyoftheUniversityofZurichandInstitute diatrics, University of California-Irvine, Irvine, for Neuroscience, Department of Health CA,UnitedStates Science and Technology, ETH Zurich, David André Barrière Physiopathologie des Switzerland Maladies Psychiatriques, UMR_S 894 Inserm, C. Neill Epperson Department of Psychiatry, Centre de Psychiatrie et Neurosciences, Paris, University of Colorado School of Medicine, France; Faculté de Médecine Paris Descartes, Aurora,CO,UnitedStates Service Hospitalo-Universitaire, Centre Hospi- talierSainte-Anne, Paris,France Edward Ganz Life and Health Sciences Research Institute (ICVS), School of Medicine, Jessica L. Bolton Department of Anatomy/ University of Minho, Braga, Portugal; ICVS/ Neurobiology, University of California-Irvine, 3B’s, PT Government Associate Laboratory, Irvine, CA, United States; Department of Pe- Braga/Guimarães,Portugal diatrics, University of California-Irvine, Irvine, CA,UnitedStates Jakob Hartmann McLean Hospital e Harvard Medical School, Mailman Research Center, Mallory E. Bowers Department of Psychiatry, Neurobiology of Fear Laboratory, Belmont, IcahnSchoolofMedicineatMountSinai,New MA,UnitedStates York,NY,UnitedStates Marloes J.A.G. Henckens Department of Dennis S. Charney Department of Psychiatry, Cognitive Neuroscience, Donders Institute for IcahnSchoolofMedicineatMountSinai,New Brain,CognitionandBehaviour,Radboudumc, York,NY,UnitedStates Nijmegen,TheNetherlands Alon Chen Department of Stress Neurobiology JamesP.Herman DepartmentofPharmacology and Behavioral Neurogenetics, Max Planck and System Physiology, University of Cincin- Institute of Psychiatry, Munich, Germany; nati,Cincinnati,OH,UnitedStates Department of Neurobiology, Weizmann Institute ofScience,Rehovot,Israel xi xii CONTRIBUTORS Matthew N. Hill Hotchkiss Brain Institute, Ricardo Magalhães Life and Health Sciences Cumming School of Medicine, University of Research Institute (ICVS), School of Medicine, Calgary,Calgary,AB,Canada University of Minho, Braga, Portugal; ICVS/ S.B. Hill Division of Depression and Anxiety, 3B’s, PT Government Associate Laboratory, Braga/Guimarães, Portugal McLean Hospital; Department of Psychiatry, HarvardMedicalSchool,Belmont,MA,United Isabelle M. Mansuy Laboratory of Neuro- States epigenetics, Brain Research Institute, Medical Brian M. Iacoviello Department of Psychiatry, facultyoftheUniversityofZurichandInstitute for Neuroscience, Department of Health IcahnSchoolofMedicineatMountSinai,New Science and Technology, ETH Zurich, York, NY, United States; Discovery and Translational Research, Click Therapeutics, Switzerland Inc.,New York,NY,UnitedStates Bruce S. McEwen Alfred E. Mirsky Professor Orna Issler Nash Family Department of Neu- Head, Harold and Margaret Milliken Hatch, Laboratory of Neuroendocrinology, The Rock- roscience and Friedman Brain Institute, Icahn SchoolofMedicineatMountSinai,NewYork, efellerUniversity,NewYork,NY,UnitedStates NY,UnitedStates Sébastien Mériaux Neurospin, JOLIOT, CEA, Thérèse M. Jay Physiopathologie des Maladies Gif-sur-Yvette, France Psychiatriques, UMR_S 894 Inserm, Centre de LaiaMorató LaboratoryofBehavioralGenetics, Psychiatrie et Neurosciences, Paris, France; Brain Mind Institute, École Polytechnique Faculté de Médecine Paris Descartes, Service Fédérale de Lausanne (EPFL), Lausanne, Hospitalo-Universitaire, Centre Hospitalier Switzerland Sainte-Anne,Paris,France Kathleen E. Morrison Department of Pharma- Marian Joëls Department of Translational Neu- cology, University ofMarylandSchool ofMed- roscience, UMC Utrecht Brain Center, Univer- icine,Baltimore,MD,UnitedStates; Centerfor sity Medical Center Utrecht, University of Epigenetic Research in Child Health and Brain Utrecht, Utrecht, The Netherlands; University Development,UniversityofMarylandSchoolof of Groningen/University Medical Center Gro- Medicine,Baltimore,MD,UnitedStates ningen,Groningen,TheNetherlands IrisMüller DepartmentofGenetics&Molecular C.D. King Division of Depression and Anxiety, Neurobiology, Institute of Biology, Otto-von- McLean Hospital; Department of Psychiatry, Guericke University Magdeburg, Magdeburg, HarvardMedicalSchool,Belmont,MA,United Germany; Department of Psychological Sci- States ences, Purdue University, Indianapolis, IN, Stafford L. Lightman Bristol Medical School: UnitedStates Translational Health Sciences, University of CharlesB.Nemeroff Department ofPsychiatry Bristol,Bristol,UnitedKingdom and Behavioral Sciences, Miller School of Ekaterina Likhtik Hunter College, The Gradu- Medicine, Miami,FL,UnitedStates ateCenter, CityUniversity ofNewYork, New Eric J. Nestler Nash Family Department of York,NY,UnitedStates Neuroscience and Friedman Brain Institute, Zachary S. Lorsch Nash Family Department of IcahnSchoolofMedicineatMountSinai,New York, NY,UnitedStates Neuroscience and Friedman Brain Institute, IcahnSchoolofMedicineatMountSinai,New OliviaF.O’Leary DepartmentofAnatomyand York,NY,UnitedStates Neuroscience, University College Cork, Cork, DavidM.Lyons Department ofPsychiatryand Ireland; APC Microbiome Institute, Univer- sityCollege Cork,Cork,Ireland Behavioral Sciences, Stanford University, Stan- ford,CA,UnitedStates xiii CONTRIBUTORS Lilia Papst Department of Translational A.V. Seligowski Division of Depression and ResearchinPsychiatry,MaxPlanckInstituteof Anxiety, McLean Hospital; Department of Psychiatry,Munich, Germany Psychiatry, Harvard Medical School, Belmont, Sachin Patel Departments of Psychiatry and MA,UnitedStates Behavioral Sciences, Pharmacology, Molecular Annabel K. Short Department of Anatomy/ Physiology & Biophysics, and The Vanderbilt Neurobiology, University of California-Irvine, Brain Institute, Vanderbilt University Medical Irvine, CA, United States; Department of Pe- Center,Nashville,TN,UnitedStates diatrics, University of California-Irvine, Irvine, Rony Paz Weizmann Institute of Science, CA,UnitedStates Rehovot,Israel Nuno Sousa Life and Health Sciences Research K.J. Ressler Division of Depression and Anxi- Institute(ICVS),SchoolofMedicine,University ety, McLean Hospital; Department of Psychia- of Minho, Braga, Portugal; ICVS/3B’s, PT Government Associate Laboratory, Braga/ try, Harvard Medical School, Belmont, MA, Guimarães,Portugal UnitedStates Gal Richter-Levin Department of Psychology, Francesca Spiga Bristol Medical School: Trans- University of Haifa, Haifa, Israel; Sagol lational Health Sciences, University of Bristol, Bristol,UnitedKingdom Department of Neurobiology, University of Haifa,Haifa,Israel; TheIntegratedBrainand Oliver Stork Department of Genetics & BehaviorResearchCenter(IBBR),Universityof Molecular Neurobiology, Institute of Biology, Haifa,Haifa, Israel Otto-von-Guericke University Magdeburg, Mariana Rodrigues Life and Health Sciences Magdeburg, Germany; Center for Behavioral BrainSciences, Magdeburg,Germany Research Institute (ICVS), School of Medicine, University of Minho, Braga, Portugal; ICVS/ SharifulA.Syed DepartmentofPsychiatryand 3B’s, PT Government Associate Laboratory, BehavioralSciences,MillerSchoolofMedicine, Braga/Guimarães,Portugal; AlgoritmiCentre, Miami,FL,UnitedStates UniversityofMinho,Braga,Portugal Kuldeep Tripathi Sagol Department of Neuro- Carmen Sandi Laboratory of Behavioral biology,University ofHaifa, Haifa,Israel Genetics, Brain Mind Institute, École Poly- Christiaan H. Vinkers VU University Medical technique Fédérale de Lausanne (EPFL), Center,Amsterdam,The Netherlands Lausanne,Switzerland A.P. Wingo Division of Depression and Anxi- R.Angela Sarabdjitsingh Department of Trans- ety, McLean Hospital; Department of Psychia- lational Neuroscience, UMC Utrecht Brain try, Harvard Medical School, Belmont, MA, Center, University Medical Center Utrecht, UnitedStates UniversityofUtrecht,Utrecht,TheNetherlands RachelYehuda DepartmentofPsychiatry,Icahn Alan F. Schatzberg Department of Psychiatry School of Medicine at Mount Sinai, New York, and Behavioral Sciences, Stanford University, NY,UnitedStates; MentalHealthCareCenter, Stanford,CA,UnitedStates JamesJ.PetersVeteransAffairsMedicalCenter, Mathias V. Schmidt Max Planck Institute of Bronx, NY, United States; Department of Neu- Psychiatry,Munich, Germany roscience, Icahn School of Medicine at Mount Sinai,NewYork,NY,UnitedStates About the editor Prof. Alon Chen is President-Elect of the Weizmann Institute of ScienceandwillbeginhistermonDecember1,2019.HewasHead of the Department of Neurobiology from 2016 to 19. He is also a Director and Scientific Member at the Max Planck Institute of Psychiatry,Munich,Germany,and serves as theHeadof the Max Planck SocietydWeizmann Institute of Science Laboratory for Experimental Neuropsychiatry and Behavioral Neurogenetics. He is an adjunct professor at the Medical School of the Ludwig Maximilian University, Munich. Prof.ChenreceivedaBScinBiologicalStudies,withdistinction, from Ben-Gurion University in 1995, and a PhD from the Weiz- mann Institute of Science in 2001 (Direct PhD Program, with distinction). During his PhD studies, Prof. Chen also received an MBAfromBen-GurionUniversity.Hewasapostdoctoralfellowat the Salk Institute for Biological Studies in California, where he started researching stress. In 2005,hejoinedthefacultyoftheWeizmannInstitute,intheDepartmentofNeurobiology.At the Weizmann Institute, he is the incumbent of the Vera and John Schwartz Family Profes- sorial Chair. Prof. Chen’s research focuses on the neurobiology of stress, particularly the mechanisms by which the brain regulates the response to stressful challenges and how this response is linkedtopsychiatricdisorders.Thecollectivelong-termgoalofhisresearchistoelucidatethe pathwaysandmechanismsbywhichstressorsareperceived,processed,andtransducedinto neuroendocrine and behavioral responses under healthy and pathological conditions. His laboratory has made significant discoveries in this field, including fundamental as- pects of the organism’s stress response and actions that link specific stress-related genes, epigenetic mechanisms, and brain circuits with anxiety disorders, depression, eating disor- ders, and the metabolic syndrome. Prof. Chen and his team use both genetic mouse models and human patients to ultimately create the scientific groundwork for therapeutic in- terventions to treat stress-related behavioral and physiological disorders. Prof. Chen is known for his excellent communication and interpersonal skills, strong leadership aptitude, and the ability to identify opportunities and to convert challenges into innovative solutions. xv Preface “Itisnotstressthatkillsus,itisourreaction an individual’s response to stressful stimuli, toit.”HansSelye(1907e1982) manifested with a susceptible or resilient outcome. Given that exposure to stressful life ex- Both humans and animals show notable periences is often unavoidable, understand- variability in their responses to stressful ingwhatmakesindividualsresilienttostress challenges. In some individuals, a major and how resilience can be built is of great acute insult or chronic stressor triggers interest and constitutes an integral part of abnormal behavioral and physiological re- preventiveandtherapeuticefforts.Sincepro- sponses and precipitates the onset of psy- resilient molecular and cellular mechanisms chiatric disease, while in most others, the can counteract the deleterious effects of same stressors have little to no effect. This stressful challenges or trauma, a better un- phenomenon of individual resistance to derstanding of resilience promoting factors stressors has been broadly termed stress and processes, as well as inter-individual resilience. Commonly, stress resilience, differences in resilience is needed. Conse- which is essential for good health and well- quently, this understanding could pave the being, refers to the individual’s ability to way for new clinical interventions for stress- retain a set of adaptive characteristics that relatedpsychopathologiesincludinganxiety, enable coping and recovery from stressful depression and post-traumatic stress disor- challenges or trauma or even enable one to der (PTSD). thrive as result of this process. To date, the field of stress neurobiology The collective and pivotal aim of the or- has largely recognized stress resilience as ganism’s response to stressors is the main- simply the absence of any psychopathology tenance of homeostasis in the presence of after an extremely stressful event or chronic real or perceived challenges. This process stress exposure.Thisbookaimsto provide a requires numerous adaptive responses broader and comprehensive overview of involvingchangesinthecentralnervousand stress resilience and presents it rather as a neuroendocrinesystems.Whenasituationis highly complex process of effective and perceived as stressful, the brain activates adaptive coping to diverse stressful or trau- many neuronal circuits, linking centers matic stimuli; a continuum of adjustable involved in sensory, motor, autonomic, physiological and behavioral changes that neuroendocrine, cognitive, and emotional shows a large inter-individual variation and functions in order to adapt to the demand can change over time. World-leading scien- posed by the threat. However, the details of tists and psychiatrists, working in the newly the pathways by which the brain translates emerging field of stress resilience, present stressful stimuli into the final, integrated and discuss the diverse biological and envi- biological response are only partially ronmental factors that shape and determine xvii xviii PREFACE understood. Nevertheless, there is extensive regions, neurochemical processes, and evidence showing that inappropriate regu- unique biomarkers. lation, disproportional intensity, or chronic Someconsiderstressresiliencetobeapre- and/or irreversible activation of the stress existingpersonalitytrait,independentofrisk response is linked to the etiology and path- exposure. Trait characteristics and assess- ophysiologyofanarrayofphysiologicaland ments suggest that cognitive capabilities, behavioral disorders. Previously, most personality, and neurobiological factors research focused on understanding what work alongside environmental factors to positions an individual at greater risk for make certain individuals more or less resil- developing stress-related disorders, but ient. Experiences that are emotionally stress- more recently the focus has shifted to those ful but not traumatic promote coping and individuals who do not develop significant build resilience since they are known to psychopathology following stress, and who enhance learning and memory mechanisms, are typically referred to as being resilient. and can be used in therapeutic settings to In several animal models and in human foster recovery and resilience. Thus, rather studies, resilience is associated with rapid than just a lack of significant psychological activation of the stress response and its effi- symptoms, we can also define resilience by cient termination. It is further characterized the specific mechanisms that help to reduce by the capacity to constrain stress-induced one’s risk of developing such symptoms. For increases in corticotropin-releasing factor example, while there is no single genetic (CRF) and cortisol through an elaborate marker that predicts the development of negative feedback system. Stress mediators, PTSD following trauma, there do appear to such as noradrenaline, the CRF family of be biological markers, mechanisms, and pro- neuropeptides, endocannabinoids or corti- cesses that help buffer the effects of trauma. costerone/cortisol, are of obvious signifi- The unique characteristics of resilient in- cance for understanding the mechanism of dividuals have gained substantial interest in resilience. A proper balance in signaling recent years, and growing efforts in animal cascades that regulate physiological re- models have attempted to unravel the mo- sponses and behavioral adaptation to a lecular and cellular mechanisms that under- stressor is key in understanding the mecha- lie this phenomenon. These animal studies nisms of resilience. Thus, for optimal resil- haveidentifiedchangesinseveralmolecules, ience, the sympathetic and parasympathetic pathways and circuits, which involve mul- nervous system, the pro- and anti- tiple brain regions. While some molecular inflammatory cytokines, and the activating pathways identified in resilience overlap and inhibiting arms of the hypothalamic- with those regulated in the opposite direc- pituitary-adrenal (HPA) axis need to be in tioninstresssusceptibility,othersareunique balance. to stress-resilient individuals. Again, this Resilience may be demonstrated by resis- suggeststhatthemolecularandcellularbasis tance to the negative effects of stressful of resilience is not merely the absence of challengesorbyrecoverytoanormalstateof susceptibility,butratheractiveandadaptive functioning more quickly than expected processes, with genetic, epigenetic, tran- following a stressful event. As such, it is scriptional, cellular and circuit ebased important to distinguish between resistance mechanisms playing important roles in to, and recovery from, stressful events, as mediating the behavioral and physiological these outcomes may involve distinct brain response to stressful challenges.
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