Specification of catecholaminergic and serotonergic neurons

The specification of neurotransmitter phenotype is an important aspect of neuronal fate determination. Substantial progress has been made in uncovering key extracellular signals and transcriptional regulators that control the mode of neurotransmission in several model systems, among which catecholaminergic and serotonergic neurons feature prominently. Here, we review our current knowledge of the regulatory circuits that direct neurotransmitter choice, and discuss the development of well-studied types of catecholaminergic and serotonergic neurons. One emerging concept is that different types of neuron use a similar core programme to control shared modes of neurotransmission, but recruit different factors that are specific for each neuronal type. Another is that most factors that specify neurotransmitter identity also control other features of the neuronal phenotype.

[1]  David J. Anderson,et al.  Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons , 1993, Cell.

[2]  H. Handa,et al.  A regulator of transcriptional elongation controls vertebrate neuronal development , 2000, Nature.

[3]  J. Rubenstein,et al.  FGF and Shh Signals Control Dopaminergic and Serotonergic Cell Fate in the Anterior Neural Plate , 1998, Cell.

[4]  M. Hirsch,et al.  Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. , 1998, Development.

[5]  J. Rubenstein,et al.  Longitudinal organization of the anterior neural plate and neural tube. , 1995, Development.

[6]  D. Ovchinnikov,et al.  Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome , 1998, Nature Genetics.

[7]  James Douglas Engel,et al.  Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system , 2000, Nature Genetics.

[8]  M. Palkovits,et al.  Nigrostriatal innervation is preserved in Nurr1-null mice, although dopaminergic neuron precursors are arrested from terminal differentiation. , 2000, Brain research. Molecular brain research.

[9]  J. Drouin,et al.  Pitx3 activates mouse tyrosine hydroxylase promoter via a high‐affinity binding site , 2001, Journal of neurochemistry.

[10]  J. Granneman,et al.  Nurr1 enhances transcription of the human dopamine transporter gene through a novel mechanism , 2001, Journal of neurochemistry.

[11]  D. Anderson,et al.  MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. , 1998, Development.

[12]  L. Olson,et al.  Cellular expression of the immediate early transcription factors Nurr1 and NGFI-B suggests a gene regulatory role in several brain regions including the nigrostriatal dopamine system. , 1996, Brain research. Molecular brain research.

[13]  T. Jessell,et al.  Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm , 1995, Cell.

[14]  A. Joyner,et al.  Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. , 1998, Development.

[15]  David J. Anderson,et al.  Alternative Neural Crest Cell Fates Are Instructively Promoted by TGFβ Superfamily Members , 1996, Cell.

[16]  H. Rohrer,et al.  Development of the cholinergic neurotransmitter phenotype in postganglionic sympathetic neurons , 1999, Cell and Tissue Research.

[17]  Randy D. Blakely,et al.  Expression cloning of a cocaine-and antidepressant-sensitive human noradrenaline transporter , 1991, Nature.

[18]  T. Perlmann,et al.  A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and NURR1. , 1995, Genes & development.

[19]  W. Wurst,et al.  mPet-1, a mouse ETS-domain transcription factor, is expressed in central serotonergic neurons , 2002, Development Genes and Evolution.

[20]  T. Jessell,et al.  A Homeodomain Protein Code Specifies Progenitor Cell Identity and Neuronal Fate in the Ventral Neural Tube , 2000, Cell.

[21]  D. Swanson,et al.  The Homeodomain Protein Arix Interacts Synergistically with Cyclic AMP to Regulate Expression of Neurotransmitter Biosynthetic Genes* , 1997, The Journal of Biological Chemistry.

[22]  Samuel L. Pfaff,et al.  Cracking the Transcriptional Code for Cell Specification in the Neural Tube , 2001, Cell.

[23]  X. Morin,et al.  Defects in Sensory and Autonomic Ganglia and Absence of Locus Coeruleus in Mice Deficient for the Homeobox Gene Phox2a , 1997, Neuron.

[24]  D. Srivastava,et al.  Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND , 1997, Nature Genetics.

[25]  M. Smidt,et al.  Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  David J. Anderson,et al.  Specification of Neurotransmitter Identity by Phox2 Proteins in Neural Crest Stem Cells , 1999, Neuron.

[27]  Chris I. De Zeeuw,et al.  GATA-3 Is Involved in the Development of Serotonergic Neurons in the Caudal Raphe Nuclei , 1999, The Journal of Neuroscience.

[28]  David J. Anderson,et al.  The bHLH Transcription Factor Olig2 Promotes Oligodendrocyte Differentiation in Collaboration with Nkx2.2 , 2001, Neuron.

[29]  G Wolterink,et al.  A homeodomain gene Ptx3 has highly restricted brain expression in mesencephalic dopaminergic neurons. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Hansson,et al.  Serotonin transporter messenger RNA in the developing rat brain: early expression in serotonergic neurons and transient expression in non-serotonergic neurons , 1998, Neuroscience.

[31]  M. Smidt,et al.  A Response Element for the Homeodomain Transcription Factor Ptx3 in the Tyrosine Hydroxylase Gene Promoter , 2000, Journal of neurochemistry.

[32]  Wolfgang Wurst,et al.  Neural plate patterning: Upstream and downstream of the isthmic organizer , 2001, Nature Reviews Neuroscience.

[33]  H. Rohrer,et al.  The specification of noradrenergic locus coeruleus (LC) neurones depends on bone morphogenetic proteins (BMPs). , 2002, Development.

[34]  R. Wingate,et al.  Tlx-1 and Tlx-3 Homeobox Gene Expression in Cranial Sensory Ganglia and Hindbrain of the Chick Embryo: Markers of Patterned Connectivity , 1998, The Journal of Neuroscience.

[35]  D. Steindler,et al.  Two types of locus coeruleus neurons born on different embryonic days in the mouse , 2004, Anatomy and Embryology.

[36]  J. Murray,et al.  Deletion in the promoter region and altered expression of Pitx3 homeobox gene in aphakia mice. , 2000, Human molecular genetics.

[37]  S. Landis Target regulation of neurotransmitter phenotype , 1990, Trends in Neurosciences.

[38]  J. D. Engel,et al.  The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. , 1999, Development.

[39]  Rudolf Nieuwenhuys,et al.  Chemoarchitecture of the Brain , 1985, Springer Berlin Heidelberg.

[40]  X. Morin,et al.  The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives , 1999, Nature.

[41]  S. Cassel,et al.  A homeodomain protein selectively expressed in noradrenergic tissue regulates transcription of neurotransmitter biosynthetic genes , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  A. Rosenthal,et al.  Specification of dopaminergic and serotonergic neurons in the vertebrate CNS , 1999, Current Opinion in Neurobiology.

[43]  F. Bloom,et al.  The biochemical basis of neuropharmacology, 2nd ed. , 1974 .

[44]  S. Landis,et al.  Cellular and molecular determinants of sympathetic neuron development. , 1999, Annual review of neuroscience.

[45]  I. Törk,et al.  Early development of serotonin‐containing neurons and pathways as seen in wholemount preparations of the fetal rat brain , 1988, The Journal of comparative neurology.

[46]  D. Rueger,et al.  Number of adrenergic and Islet‐1 immunoreactive cells is increased in avian trunk neural crest cultures in the presence of human recombinant osteogenic protein‐1 , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[47]  R. Palmiter,et al.  Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic , 1995, Cell.

[48]  K. Mizuseki,et al.  Induction of Midbrain Dopaminergic Neurons from ES Cells by Stromal Cell–Derived Inducing Activity , 2000, Neuron.

[49]  M. Palkovits,et al.  Dopamine Biosynthesis Is Selectively Abolished in Substantia Nigra/Ventral Tegmental Area but Not in Hypothalamic Neurons in Mice with Targeted Disruption of the Nurr1 Gene , 1998, Molecular and Cellular Neuroscience.

[50]  J. Brunet,et al.  Paired‐Like Homeodomain Proteins, Phox2a and Phox2b, Are Responsible for Noradrenergic Cell‐Specific Transcription of the Dopamine β‐Hydroxylase Gene , 1998, Journal of neurochemistry.

[51]  H. Rohrer,et al.  The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. , 2000, Development.

[52]  J. Barker,et al.  Early appearance of tyrosine hydroxylase immunoreactive cells in the mesencephalon of mouse embryos , 1990, International Journal of Developmental Neuroscience.

[53]  L. Olson,et al.  Orphan Nuclear Receptor Nurr1 Is Essential for Ret Expression in Midbrain Dopamine Neurons and in the Brain Stem , 2001, Molecular and Cellular Neuroscience.

[54]  Kwang-Soo Kim,et al.  A direct role of the homeodomain proteins Phox2a/2b in noradrenaline neurotransmitter identity determination , 2002, Journal of neurochemistry.

[55]  R. McKay,et al.  Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells , 2000, Nature Biotechnology.

[56]  S. Shirasawa,et al.  Formation of brainstem (nor)adrenergic centers and first-order relay visceral sensory neurons is dependent on homeodomain protein Rnx/Tlx3. , 2001, Genes & development.

[57]  J. Rubenstein,et al.  Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling , 1999, Nature.

[58]  H. Rohrer,et al.  Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. , 1996, Development.

[59]  T. Jessell Neuronal specification in the spinal cord: inductive signals and transcriptional codes , 2000, Nature Reviews Genetics.

[60]  D. Foster,et al.  Expression of HAND gene products may be sufficient for the differentiation of avian neural crest-derived cells into catecholaminergic neurons in culture. , 1999, Developmental biology.

[61]  E. Deneris,et al.  The ETS Domain Factor Pet-1 Is an Early and Precise Marker of Central Serotonin Neurons and Interacts with a Conserved Element in Serotonergic Genes , 1999, The Journal of Neuroscience.

[62]  A. Brivanlou,et al.  Neural patterning in the vertebrate embryo. , 2001, International review of cytology.

[63]  X. Morin,et al.  Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. , 1997, Development.

[64]  F. Gage,et al.  Nurr1, an orphan nuclear receptor, is a transcriptional activator of endogenous tyrosine hydroxylase in neural progenitor cells derived from the adult brain. , 1999, Development.

[65]  H. Rohrer,et al.  The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. , 1999, Development.

[66]  Wolfgang Wurst,et al.  Fate of Midbrain Dopaminergic Neurons Controlled by the Engrailed Genes , 2001, The Journal of Neuroscience.

[67]  H. Rohrer,et al.  The expression of tyrosine hydroxylase and the transcription factors cPhox-2 and Cash-1: evidence for distinct inductive steps in the differentiation of chick sympathetic precursor cells , 1995, Mechanisms of Development.

[68]  J. Brunet,et al.  Phox2 genes - from patterning to connectivity. , 2002, Current opinion in genetics & development.

[69]  M. Tiveron,et al.  The Expression Pattern of the Transcription Factor Phox2 Delineates Synaptic Pathways of the Autonomic Nervous System , 1996, The Journal of Neuroscience.

[70]  Marten P. Smidt,et al.  A second independent pathway for development of mesencephalic dopaminergic neurons requires Lmx1b , 2000, Nature Neuroscience.

[71]  L. Niswander,et al.  Expression of a constitutively active type I BMP receptor using a retroviral vector promotes the development of adrenergic cells in neural crest cultures. , 1998, Developmental biology.

[72]  C. Goridis,et al.  Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. , 2000, Development.

[73]  B. Joseph,et al.  Induction of Cell Cycle Arrest and Morphological Differentiation by Nurr1 and Retinoids in Dopamine MN9D Cells* , 2001, The Journal of Biological Chemistry.

[74]  E. Snyder,et al.  Induction of a midbrain dopaminergic phenotype in Nurr1-overexpressing neural stem cells by type 1 astrocytes , 1999, Nature Biotechnology.

[75]  C. Goridis,et al.  Specification of the Central Noradrenergic Phenotype by the Homeobox Gene Phox2b , 2000, Molecular and Cellular Neuroscience.

[76]  P. Gaspar,et al.  Transient developmental expression of monoamine transporters in the rodent forebrain , 1998 .

[77]  M. Adachi,et al.  Paired-like homeodomain proteins Phox2a/Arix and Phox2b/NBPhox have similar genetic organization and independently regulate dopamine beta-hydroxylase gene transcription. , 2000, DNA and cell biology.

[78]  G. Paxinos The Rat nervous system , 1985 .

[79]  L. Olson,et al.  Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. , 1999, Experimental cell research.

[80]  O. Conneely,et al.  Selective Agenesis of Mesencephalic Dopaminergic Neurons in Nurr1-Deficient Mice , 1999, Experimental Neurology.

[81]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[82]  H. Rohrer Nonneuronal cells from chick sympathetic and dorsal root sensory ganglia express catecholamine uptake and receptors for nerve growth factor during development , 1985 .

[83]  M. Placzek The role of the notochord and floor plate in inductive interactions. , 1995, Current opinion in genetics & development.

[84]  Stephen W. Wilson,et al.  Development of Noradrenergic Neurons in the Zebrafish Hindbrain Requires BMP, FGF8, and the Homeodomain Protein Soulless/Phox2a , 1999, Neuron.

[85]  David J. Anderson,et al.  The determination of the neuronal phenotype , 1997 .

[86]  J. Cubells,et al.  A Previously Undescribed Intron and Extensive 5′ Upstream Sequence, but Not Phox2a-mediated Transactivation, Are Necessary for High Level Cell Type-specific Expression of the Human Norepinephrine Transporter Gene* , 1999, The Journal of Biological Chemistry.

[87]  B J Hoffer,et al.  Dopamine neuron agenesis in Nurr1-deficient mice. , 1997, Science.

[88]  M. Wegner,et al.  Bone Morphogenetic Proteins Are Required In Vivo for the Generation of Sympathetic Neurons , 1999, Neuron.

[89]  C. Goridis,et al.  Transcriptional control of neurotransmitter phenotype , 1999, Current Opinion in Neurobiology.

[90]  E. T. Pierce Time of origin of neurons in the brain stem of the mouse. , 1973, Progress in brain research.

[91]  J. D. Engel,et al.  Differential regulation of transcription factor gene expression and phenotypic markers in developing sympathetic neurons. , 1995, Development.

[92]  U. Dräger,et al.  High levels of a retinoic acid-generating dehydrogenase in the meso-telencephalic dopamine system. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[93]  J. Brunet,et al.  Noradrenergic-Specific Transcription of the Dopamine β-Hydroxylase Gene Requires Synergy of MultipleCis-Acting Elements Including at Least Two Phox2a-Binding Sites , 1998, The Journal of Neuroscience.

[94]  A. Sidow,et al.  A double-deletion mutation in the Pitx3 gene causes arrested lens development in aphakia mice. , 2001, Genomics.

[95]  G. D. Maxwell,et al.  BMP-2 and BMP-4, but Not BMP-6, Increase the Number of Adrenergic Cells Which Develop in Quail Trunk Neural Crest Cultures , 1996, Experimental Neurology.

[96]  S. Wilson,et al.  Bmp activity establishes a gradient of positional information throughout the entire neural plate. , 1999, Development.

[97]  M. Adachi,et al.  The Homeodomain Protein Arix Promotes Protein Kinase A-dependent Activation of the Dopamine β-Hydroxylase Promoter through Multiple Elements and Interaction with the Coactivator cAMP-response Element-binding Protein-binding Protein* , 2000, The Journal of Biological Chemistry.