Patterning and Cell Type Specification in the Developing CNS and PNS: Comprehensive Developmental Neuroscience

1084 Pages·2020·64.65 MB·English

by  John Rubenstein (editor), Pasko Rakic (editor), Bin Chen (editor), Kenneth Y. Kwan (editor)

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
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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