Patterning and Cell Type Specification in the Developing CNS and PNS: Comprehensive Developmental Neuroscience PDF
Preview Patterning and Cell Type Specification in the Developing CNS and PNS: Comprehensive Developmental Neuroscience
Patterning and Cell Type Specification in the Developing CNS and PNS Comprehensive Developmental Neuroscience Second Edition Senior Editors-in-Chief John Rubenstein Department of Psychiatry & Weill Institute for Neurosciences University of California, San Francisco, San Francisco, CA, United States Pasko Rakic Department of Neuroscience & Kavli Institute for Neuroscience Yale School of Medicine, New Haven, CT, United States Editors-in-Chief Bin Chen Department of Molecular, Cell & Developmental Biology University of California, Santa Cruz, Santa Cruz, CA, United States Kenneth Y. Kwan Michigan Neuroscience Institute & Department of Human Genetics University of Michigan, Ann Arbor, MI, United States Section Editors: Elizabeth A. Grove Department of Neurobiology & Grossman Institute for Neuroscience University of Chicago, Chicago, IL, United States Shubha Tole Department of Biological Sciences Tata Institute of Fundamental Research, Mumbai, India Francois Guillemot The Francis Crick Institute, London, United Kingdom Kenneth Campbell Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center University of Cincinnati College of Medicine, Cincinnati, OH, United States Arturo Alvarez-Buylla Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research University of California, San Francisco, San Francisco, CA, United States David Rowitch Department of Paediatrics, University of Cambridge and Wellcome-MRC Cambridge Stem Cell Institute, Cambridge, United Kingdom Adjunct Professor of Pediatrics, UCSF Academic PressisanimprintofElsevier 125London Wall,LondonEC2Y5AS,UnitedKingdom 525BStreet,Suite1650,SanDiego,CA92101,UnitedStates 50HampshireStreet,5thFloor,Cambridge,MA02139,UnitedStates TheBoulevard,Langford Lane,Kidlington,OxfordOX5 1GB,UnitedKingdom Copyright©2020ElsevierInc. 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LibraryofCongressCataloging-in-Publication Data Acatalogrecord forthisbook isavailablefromtheLibrary ofCongress BritishLibraryCataloguing-in-Publication Data Acataloguerecord forthisbook isavailablefromtheBritishLibrary ISBN:978-0-12-814405-3 Forinformation onallAcademic Presspublications visitour website athttps://www.elsevier.com/books-and-journals Publisher:NikkiLevy Acquisitions Editor: NatalieFarra EditorialProjectManager:AndraeAkeh ProductionProjectManager:SuryaNarayanan Jayachandran CoverDesigner: DavidTastad TypesetbyTNQTechnologies Contributors Katerina Akassoglou, Gladstone Institute of Neurological Aparna Bhaduri, UniversityofCalifornia,SanFrancisco, Disease and Department of Neurology, University of CA, United States California, San Francisco, CA, United States S. Blaess, Institute of Reconstructive Neurobiology, LIFE NicolaJ.Allen,MolecularNeurobiologyLaboratory,Salk &BRAINCenter,UniversityofBonn,MedicalFaculty Institute for Biological Studies, La Jolla, CA, United and University Hospital Bonn, Bonn, Germany States Stephanie Bonney, Department of Pediatrics, Section of Fernando C. Alsina, Department of Molecular Genetics Developmental Biology, University of Colorado, and Microbiology Anschutz Medical Campus, Aurora, CA, United States Alessandro Alunni, Zebrafish Neurogenetics Unit, BernadettBosze,DepartmentofCellBiologyandHuman Developmental & Stem Cell Biology Department, Anatomy, University of California Davis, Davis, CA, Institut Pasteur, UMR3738, CNRS, Paris, France United States A. Alvarez-Buylla, University of California, San Fran- Joshua J. Breunig, Board of Governors Regenerative cisco, CA, United States Medicine Institute, Los Angeles, CA, United States; Department of Biomedical Sciences, Los Angeles, CA, Madeline G. Andrews, University of California, San United States; Samuel Oschin Comprehensive Cancer Francisco, CA, United States Institute, Los Angeles, CA, United States; Department S.-L. Ang, Francis Crick Institute, London, United ofMedicine,DavidGeffenSchoolofMedicine,UCLA, Kingdom Los Angeles, CA, United States B. Appel, University of Colorado School of Medicine, Nadean L. Brown, Department of Cell Biology and Hu- Aurora, CO, United States man Anatomy, University of California Davis, Davis, Badrul Arefin, Department of Clinical and Experimental CA, United States Medicine, Linköping University, Linköping, Sweden S.A. Buffington, Baylor College of Medicine, Houston, Shahrzad Bahrampour, Department of Clinical and TX, United States Experimental Medicine, Linköping University, Link- C.L. Call, Johns Hopkins School of Medicine, Baltimore, öping, Sweden MD, United States Q.-R. Bai, Tongji University, Shanghai, China K. Campbell, Cincinnati Children’s Hospital Medical Laure Bally-Cuif, Zebrafish Neurogenetics Unit, Devel- Center, University of Cincinnati College of Medicine, opmental & Stem Cell Biology Department, Institut Cincinnati, OH, United States Pasteur, UMR3738, CNRS, Paris, France Astrid E. Cardona, UTSA Brain Health Consortium and RenataBatista-Brito,DominickP.PurpuraDepartmentof South Texas Center for Emerging Infectious Diseases, Neuroscience, Albert Einstein College of Medicine, DepartmentofBiology,TheUniversityofTexasatSan Bronx, NY, United States Antonio, San Antonio, TX, United States Magnus Baumgardt, Department of Clinical and Exper- CatarinaCatela,DepartmentofNeurobiology,University imental Medicine, Linköping University, Linköping, of Chicago, Chicago, IL, United States Sweden A. Cebrián-Silla, University of California, San Francisco, Jonathan Benito-Sipos, Departamento de Biología, Uni- CA, United States; Univeristat de València, versidad Autónoma de Madrid, Madrid, Spain CIBERNED, Valencia, Spain D.E. Bergles, Johns Hopkins School of Medicine, Balti- more, MD, United States xxi xxii Contributors Yi-TingCheng,CenterforCellandGeneTherapy,Baylor Elizabeth A. Grove, Department of Neurobiology, The College of Medicine, One Baylor Plaza, Houston, TX, Grossman Institute for Neuroscience, University of United States Chicago, Chicago, IL, United States Victor V. Chizhikov, University of Tennessee Health J.L. Haigh, University of California, Davis, CA, United Science Center, Department of Anatomy and Neuro- States biology, Memphis, TN, United States Jean Hébert, Neuroscience, Genetics, Stem Cells, Albert Marion Coolen, Zebrafish Neurogenetics Unit, Devel- EinsteinCollegeofMedicine,Bronx,NY,UnitedStates opmental & Stem Cell Biology Department, Institut Oliver Hobert, Department of Biological Sciences, Pasteur, UMR3738, CNRS, Paris, France Howard Hughes Medical Institute, Columbia Univer- Jesús Rodriguez Curt, Department of Clinical and sity, New York, NY, United States Experimental Medicine, Linköping University, Robert B. Hufnagel, Medical Genetics and Ophthalmic Linköping, Sweden Genomics Unit, National Eye Institute, Bethesda, MD, Dimitrios Davalos, Neuroinflammation Research Center, United States Department of Neurosciences, Lerner Research Insti- Wieland B. Huttner, Max Planck Institute of Molecular tute, Cleveland Clinic, Cleveland, OH, United States Cell Biology and Genetics, Dresden, Germany L.M. De Biase, Johns Hopkins School of Medicine, Bal- YasuhiroItoh,DepartmentofStemCellandRegenerative timore, MD, United States Biology, and Center for Brain Science, Harvard Uni- Benjamin Deneen, Center for Cell and Gene Therapy, versity, Cambridge, MA, United States Department of Neuroscience, Baylor College of Medi- K.R. Jessen, University College London, London, United cine, One Baylor Plaza, Houston, TX, United States Kingdom Omer Durak, Department of Stem Cell and Regenerative JaneE.Johnson,DepartmentofNeuroscience,University Biology, and Center for Brain Science, Harvard Uni- of Texas Southwestern Medical Center, Dallas, TX, versity, Cambridge, MA, United States United States Ryann M. Fame, Department of Stem Cell and Regener- EyalKarzbrun,KavliInstituteofTheoreticalPhysicsand ative Biology, and Center for Brain Science, Harvard Department of Physics, University of California, Santa University,Cambridge,MA,UnitedStates;Department Barbara, CA, United States ofPathology,BostonChildren’sHospital,Boston,MA, YutaroKomuro,DepartmentofNeurology,DavidGeffen United States School of Medicine, University of California, Los Stephen P.J. Fancy, Neurology and Pediatrics, University Angeles, Los Angeles, CA, United States ofCalifornia,SanFrancisco,SanFrancisco,CA,United Hitoshi Komuro, Department of Neuroscience, Yale States University School of Medicine, New Haven, CT, Gord Fishell, Department of Neurobiology, Blavatnik United States Institute,HarvardMedicalSchool,Boston,MA,United Arnold R. Kriegstein, University of California, San States; Stanley Center for Psychiatric Research, Broad Francisco, CA, United States Institute, Cambridge, MA, United States Isabelle Foucher, Zebrafish Neurogenetics Unit, Devel- J.T.Lambert,UniversityofCalifornia,Davis,CA,United opmental & Stem Cell Biology Department, Institut States Pasteur, UMR3738, CNRS, Paris, France Katherine R. Long, Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany L. Fuentealba, University of California, San Francisco, CA, United States GuillerminaLópez-Bendito,InstitutodeNeurocienciasde Alicante, Universidad Miguel Hernández-Consejo Su- Fred H. Gage, Salk Institute for Biological Studies, La perior de Investigaciones Científicas (UMH-CSIC), Jolla, CA, United States Sant Joan d’Alacant, Spain Ludovic Galas, Normandie University, UNIROUEN, Jessica L. MacDonald, Department of Stem Cell and INSERM, PRIMACEN, Mont-Saint-Aignan, France Regenerative Biology, and Center for Brain Science, Andrew W. Grande, Department of Neurosurgery, Harvard University, Cambridge, MA, United States; University of Minnesota, Minneapolis, MN, United DepartmentofBiology,Syracuse University,Syracuse, States NY, United States Contributors xxiii Jeffrey D. Macklis, Department of Stem Cell and Regen- Masato Nakafuku, Division of Developmental Biology, erative Biology, and Center for Brain Science, Harvard Cincinnati Children’s Hospital Medical Center, De- University, Cambridge, MA, United States; Bauer partmentsofPediatricsandNeurosurgery,Universityof Laboratory, Cambridge, MA, United States CincinnatiCollegeofMedicine,Cincinnati,OH,United States Maria Carolina Marchetto, Salk Institute for Biological Studies, La Jolla, CA, United States Harukazu Nakamura, Laboratory of Organ Morpho- genesis, Graduate School of Life Sciences, Tohoku Francisco J. Martini, Instituto de Neurociencias de Ali- University, Aoba-ku, Sendai, Japan cante,UniversidadMiguelHernández-ConsejoSuperior de Investigaciones Científicas (UMH-CSIC), Sant Joan BrandenR.Nelson,CenterforIntegrativeBrainResearch, d’Alacant, Spain Seattle Children’s Research Institute, Seattle, WA, Michael P. Matise, Department of Neuroscience & Cell United States Biology, Rutgers-Robert Wood Johnson Medical A.S. Nord, University of California, Davis, CA, United School, Piscataway, NJ, United States States F.T. Merkle, Metabolic Research Laboratories and K.Obernier,UniversityofCalifornia,SanFrancisco,CA, Medical Research Council Metabolic Diseases Unit, United States Wellcome Trust-Medical Research Council Institute of Nobuhiko Ohno, Department of Anatomy, Division of Metabolic Science, and the Wellcome Trust-Medical Histology and Cell Biology, Jichi Medical University, Research Council Cambridge Stem Cell Institute, Uni- Shimotsuke-Shi, Tochigi, Japan; Division of Ultra- versity of Cambridge, Cambridge, United Kingdom structural Research, NationalInstitute for Physiological A. Meunier, Institut National de la Santé et de la Sciences, Okazaki, Aichi, Japan Recherche Médicale, Paris, France; Centre National de Abdulkadir Ozkan, Department of Stem Cell and la Recherche Scientifique, Paris, France; Institut de Regenerative Biology, and Center for Brain Science, Biologie de l’Ecole Normale Supérieure (IBENS), Harvard University, Cambridge, MA, United States Paris, France David B. Parkinson, Medicine and Dentistry, Plymouth Kathleen J. Millen, Seattle Children’s Hospital Research University, Plymouth, Devon, United Kingdom Institute Center for Integrative Brain Research, Seattle, ManuelPeter,Department of Stem Cell andRegenerative WA, United States Biology, and Center for Brain Science, Harvard Robert H. Miller, Anatomy and Cell Biology, School of University, Cambridge, MA, United States Medicine and Health Sciences, George Washington Samuel J. Pleasure, Department of Neurology, Programs University, Washington, DC, United States in Neuroscience and Developmental Biology, Institute R. Mirsky, University College London, London, United for Regenerative Medicine, University of California, Kingdom San Francisco, CA, United States Swati Mishra, Department of Pediatrics, Section of M.N.Rasband,BaylorCollegeofMedicine,Houston,TX, Developmental Biology, University of Colorado, United States AnschutzMedicalCampus,Aurora,CA,UnitedStates; Department of Pathology, Institute for Stem Cell & Orly Reiner, Department of Molecular Genetics, The Weizmann Institute of Science, Rehovot, Israel Regenerative Medicine, University of Washington, Seattle, WA, United States D.H. Rowitch, University of California, San Francisco, CA, United States Anna Victoria Molofsky, Laboratory of Molecular Neurobiology,CentreofNewTechnologies,University J.L.R. Rubenstein, University of California at San Fran- of Warsaw, Warsaw, Poland cisco, San Francisco, CA, United States Ignacio Monedero Cobeta, Department of Clinical and Debosmita Sardar, Center for Cell and Gene Therapy, Experimental Medicine, Linköping University, Baylor College of Medicine, One Baylor Plaza, Hous- Linköping, Sweden ton, TX, United States K.Monk,VollumInstitute,OregonHealthScienceCenter, Anindita Sarkar, Salk Institute for Biological Studies, La Portland, OR, United States Jolla, CA, United States Edwin S. Monuki, Pathology & Laboratory Medicine, K.Sawamoto,NagoyaCityUniversityGraduateSchoolof Developmental & Cell Biology, University of Califor- MedicalSciences,Nagoya,Japan;NationalInstitutefor nia Irvine, Irvine, CA, United States Physiological Sciences, Okazaki, Japan xxiv Contributors KamalSharma, Department of Anatomy & Cell Biology, S. Temple, Neural Stem Cell Institute, Rensselaer, NY, University of Illinois at Chicago, Chicago, IL, United United States States Stefan Thor, Department of Clinical and Experimental Q. Shen, Tongji University, Shanghai, China Medicine, Linköping University, Linköping, Sweden; School of Biomedical Sciences, University of Queens- JulieA.Siegenthaler,DepartmentofPediatrics,Sectionof land, St Lucia, QLD, Australia Developmental Biology, University of Colorado, Anschutz Medical Campus, Aurora, CA, United States Shubha Tole, Department of Biological Sciences, Tata Institute of Fundamental Research, Mumbai, Mahara- Debra L. Silver, Department of Molecular Genetics and shtra, India Microbiology;DepartmentofCellBiology;Department of Neurobiology; Duke Institute for Brain Sciences, Gregorio Valdez, Brown University, Providence, RI, Duke University Medical Center, Durham, NC, United United States States David Vaudry, Normandie University, UNIROUEN, N.Spassky,InstitutNationaldelaSantéetdelaRecherche INSERM, PRIMACEN, Mont-Saint-Aignan, France; Médicale, Paris, France; Centre National de la Recher- NormandieUniversity,UNIROUEN,INSERM,U1239, che Scientifique, Paris, France; Institut de Biologie de DC2N, Mont-Saint-Aignan, France l’Ecole Normale Supérieure (IBENS), Paris, France Claire Ward, Dominick P. Purpura Department of Neu- S.R.W.Stott,TheCureParkinson’sTrust,London,United roscience, Albert Einstein College of Medicine, Bronx, Kingdom NY, United States Johannes Stratmann, Department of Clinical and Exper- Michael Wegner, Institut für Biochemie, Emil-Fischer- imental Medicine, Linköping University, Linköping, Zentrum, Universität Erlangen-Nürnberg, Erlangen, Sweden Germany L. Subramanian, University of California, San Francisco, BehzadYaghmaeianSalmani,DepartmentofClinicaland CA, United States Experimental Medicine, Linköping University, Linköping, Sweden JohnSvaren,DepartmentofComparativeBiosciencesand Waisman Center, University of Wisconsin, Madison, WI, United States LukaszMateusz Szewczyk,DepartmentofPsychiatryand WeillInstituteforNeurosciences,UniversityofCalifor- nia, San Francisco, San Francisco, CA, United States; Laboratory of Molecular Neurobiology, Centre of New Technologies, University of Warsaw, Warsaw, Poland Chapter 1 Morphogens, patterning centers, and their mechanisms of action Elizabeth A. Grove1 and Edwin S. Monuki2 1DepartmentofNeurobiology,UniversityofChicago,Chicago,IL,UnitedStates;2Pathology&LaboratoryMedicine,Developmental&Cell Biology,UniversityofCaliforniaIrvine,Irvine,CA,UnitedStates Chapter outline 1.1. Generalprinciplesofmorphogengradients 3 1.3.2. Midlineexpressionandhomeogeneticexpansionof 1.1.1. Historyofthemorphogenandmorphogeneticfield 3 BMPproduction 10 1.1.2. Howmorphogengradientspatterntissues 4 1.3.3. BMPsignalinggradientinthedorsaltelencephalon 11 1.1.3. Howmorphogensaredistributed 5 1.3.4. BMPsasdorsaltelencephalicmorphogens 11 1.1.4. Howmorphogensignalingistransducedand 1.3.5. LinearconversionofBMPsignalingbycorticalcells 12 interpreted 6 1.3.6. NonlinearconversionofBMPsignalingbyDTM 1.1.5. Howmorphogengradientsareconvertedintosharp cells 12 boundaries 6 1.3.7. SummarydtheBMPsignalinggradient 13 1.1.6. Summarydgeneralprinciplesofmorphogen 1.4. FGF8asamorphogenintelencephalicpatterning 13 gradients 7 1.5. Interactionsamongsignalingcentersintelencephalic 1.2. Localsignalingcentersandprobablemorphogensinthe patterning 14 telencephalon 7 1.5.1. FGF8,Shh,andBMPsignaling 15 1.2.1. Earlyforebrainpatterning 8 1.5.2. Cross-regulationofBMP,FGF,andWNTsignaling 15 1.2.2. TheRPC 8 1.5.3. InteractionsofShh,FGFs,andGli3 15 1.2.3. Thetelencephalicroofplateandcorticalhem 8 1.6. Morphogensinhumanbraindisease 15 1.2.4. Theantihem 9 1.6.1. HoloprosencephalyandKallmannsyndrome 15 1.3. BMPsasmorphogensintelencephalicpatterning 9 1.6.2. Gradientsinholoprosencephalyneuropathology 17 1.3.1. PerformanceobjectivesforaBMPgradientinthe 1.6.3. Gradientsinotherhumanbraindisorders 17 dorsaltelencephalon 9 References 18 1.1 General principles of morphogen gradients 1.1.1 History of the morphogen and morphogenetic field The concept of a morphogen can be traced to the turn of the 20th century, when Morgan postulated the presence of “formativesubstances”asthebasisfordifferentregenerationratesinworms(Morgan,1901).Verysoonthereafter,Boveri entertainedthisideafornormaldevelopment(Boveri,1901).Aseminaleventforthisfieldwasthediscoveryofalocalized source for morphogens known as the Spemann organizer (Spemann and Mangold, 1924). The term “morphogen” was coinedbyTuring,whodescribedhowuniformlydistributedsignalsmadebycellscanspread,self-organize,andgenerate pattern (Turing, 1952). Turing patterns remain highly relevant in development, but for this chapter and the developing forebrain, the more relevant concept is that of nonuniform graded distributions of morphogens, an idea formalized in the famous “French flag” model of Wolpert (Fig. 1.1) (Wolpert, 1969). 3 PatterningandCellTypeSpecificationintheDevelopingCNSandPNS.https://doi.org/10.1016/B978-0-12-814405-3.00001-1 Copyright©2020ElsevierInc.Allrightsreserved. 4 PART | I InductionandpatterningoftheCNSandPNS n e g o h p or 2 M 1 Distance from source FIGURE1.1 TheFrenchflagmodel.Schematicofhowadiffusiblemorphogencanassignpositionalvaluesandinstructcellsfates.Morphogen(green) secreted from a source cell forms a concentration gradient within a tissue. At intermediate concentrations above threshold 1, responding cells adopt “white”fate.Athighconcentrationsabovethreshold2,cellsadopt“blue”fate.BasedonKicheva,A.,Gonzalez-Gaitan,M.,2008.TheDecapentaplegic morphogengradient:aprecisedefinition.Curr.Opin.CellBiol.20,137e143;Rogers,K.W.,Schier,A.F.,2011.Morphogengradients:fromgeneration tointerpretation.Annu.Rev.CellDev.Biol.27,377e407. In this model, Wolpert described smoothly declining gradients of morphogen concentration within a “morphogenetic field”ofcells.Thesegradientswereimaginedtoariseviadiffusionfromalocalizedsourcetowardasink,thusgivingcells within the morphogenetic field different positional values based on morphogen concentration. The positional values then determined the fates adopted by cells in the field (Fig. 1.1). It was not until the 1980s that the molecular identity of a morphogen was defined (bicoid) (Driever and Nusslein-Volhard, 1988a, 1988b). The first secreted morphogen was identified soon thereafter (decapentaplegic or dpp) (Ferguson and Anderson, 1992). Since then, many more morphogens have been discovered. Most, but not all, are secreted proteins; examples of other molecular classes include transcription factors (bicoid and dorsal) and a vitamin derivative (retinoic acid). 1.1.2 How morphogen gradients pattern tissues Theconceptofpositionalidentityisimportantforunderstandinghowmorphogengradientsworkbecauseitiserroneousto consider morphogens as the sole determinants of cell fate. As it turns out, the same limited repertoire of morphogens is usedoverandoveragainacross ontogenyandphylogenytogeneratethedizzyingarray ofcelltypes found intheanimal kingdom. Thus, morphogens could not possibly be instructive of cell fate on their own. Rather, morphogens act upon tissueswithdifferentprepatternsandcompetencies,andthesecompetenciesincombinationwiththepositionalinformation provided by morphogens determine cell fate. For example, in this chapter, we discuss in detail how bone morphogenetic proteins (BMPs, the orthologues of dpp) and fibroblast growth factors (FGFs) provide positional information to dorsal telencephalic cells with restricted neural potential. The defining property of a morphogen is the ability to specify two or more cell fates in a concentration-dependent manner. For some, at least three fates are necessary to ensure that a morphogen is truly instructive (Freeman and Gurdon,2002).Morphogensoftenspecifybetweenthreetosevenfateswithinatissue(AsheandBriscoe,2006),whichare separated by sharp, discrete boundaries. The acquisition of mature cell fates and boundaries is preceded by cell-intrinsic differencesintheexpressionof“selector”genes(mostoftentranscriptionfactors)thatspecifycellfatesinparticularways (Garcia-Bellido, 1975). Understanding how graded morphogenic information is converted into sharp (switch-like or ultrasensitive) changes indownstream geneexpressionremains acentral problemfor developmentalbiologists, although, as we will see below, several mechanisms underlying such “switches” have been defined. One important objective for many tissues patterned by morphogens is the establishment of secondary organizers or signaling centers (Meinhardt, 2009). These secondary sites of morphogen production expand the ranges over which morphogens can act, provide for finer subdivisions of pattern, or both, and are located at boundaries established by the primarymorphogengradientandselectorgenes.Otherconsequencesofprimarypatterningincludeapoptosis,cellsorting tofurtherrefineborders,andotherformsofcell-to-cellsignaling(Landeretal.,2009a).Theseeventscanberegulatedby morphogens or may become largely cell-autonomous and immune to extrinsic control. An interesting potential use of
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