Multicluster Pcdh diversity is required for mouse olfactory neural circuit assembly
The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters (Pcdhα, Pcdhβ, and Pcdhγ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface divers...
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| Published in | Science (American Association for the Advancement of Science) Vol. 356; no. 6336; pp. 411 - 414 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Association for the Advancement of Science
28.04.2017
The American Association for the Advancement of Science |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0036-8075 1095-9203 1095-9203 |
| DOI | 10.1126/science.aai8801 |
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| Abstract | The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters (Pcdhα, Pcdhβ, and Pcdhγ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual Pcdh clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single–tricluster gene repertoire (α and β and γ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms. |
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| AbstractList | Pattern formation in the brain: Neurons in the developing brain cooperate to build circuits. Mountoufaris et al. found that similar to 50 variable protocadherin genes support a combinatorial identity code that allows millions of olfactory neuron axons to sort into similar to 2000 glomeruli. Sharing olfactory receptors drives axons to one glomerulus, and protocadherin diversity allows the multiple axons to touch each other as they converge. On the other hand, Chen et al. found that a single C-type protocadherin underlies the tiled distribution of serotonergic neurons throughout the central nervous system. These neurons, which share protocadherin identity, enervate broad swaths evenly without touching neighboring neurons.Science, this issue p. 411, p. 406 The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters (Pcdh alpha , Pcdh beta , and Pcdh gamma ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual Pcdh clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single-tricluster gene repertoire ( alpha and beta and gamma ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms. Neurons in the developing brain cooperate to build circuits. Mountoufaris et al. found that ∼50 variable protocadherin genes support a combinatorial identity code that allows millions of olfactory neuron axons to sort into ∼2000 glomeruli. Sharing olfactory receptors drives axons to one glomerulus, and protocadherin diversity allows the multiple axons to touch each other as they converge. On the other hand, Chen et al. found that a single C-type protocadherin underlies the tiled distribution of serotonergic neurons throughout the central nervous system. These neurons, which share protocadherin identity, enervate broad swaths evenly without touching neighboring neurons. Science , this issue p. 411 , p. 406 Genetic approaches in mice reveal the functional importance of the multicluster organization of mammalian protocadherin genes. The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters ( Pcdh α, Pcdh β, and Pcdh γ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual Pcdh clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single–tricluster gene repertoire (α and β and γ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms. The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters ( Pcdh α, Pcdh β, and Pcdh γ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual Pcdh clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single–tricluster gene repertoire (α and β and γ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms. The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters ( α, β, and γ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single-tricluster gene repertoire (α and β and γ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms. Neurons in the developing brain cooperate to build circuits. Mountoufaris et al. found that ∼50 variable protocadherin genes support a combinatorial identity code that allows millions of olfactory neuron axons to sort into ∼2000 glomeruli. Sharing olfactory receptors drives axons to one glomerulus, and protocadherin diversity allows the multiple axons to touch each other as they converge. On the other hand, Chen et al. found that a single C-type protocadherin underlies the tiled distribution of serotonergic neurons throughout the central nervous system. These neurons, which share protocadherin identity, enervate broad swaths evenly without touching neighboring neurons. Science, this issue p. 411, p. 406 The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters (Pcdhα, Pcdhβ, and Pcdhγ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual Pcdh clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single-tricluster gene repertoire (α and β and γ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms. The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters (Pcdhα, Pcdhβ, and Pcdhγ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual Pcdh clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single–tricluster gene repertoire (α and β and γ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms. The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters (Pcdhα, Pcdhβ, and Pcdhγ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual Pcdh clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single-tricluster gene repertoire (α and β and γ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms.The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters (Pcdhα, Pcdhβ, and Pcdhγ). Here, we show that all three gene clusters functionally cooperate to provide individual mouse olfactory sensory neurons (OSNs) with the cell surface diversity required for their assembly into distinct glomeruli in the olfactory bulb. Although deletion of individual Pcdh clusters had subtle phenotypic consequences, the loss of all three clusters (tricluster deletion) led to a severe axonal arborization defect and loss of self-avoidance. By contrast, when endogenous Pcdh diversity is overridden by the expression of a single-tricluster gene repertoire (α and β and γ), OSN axons fail to converge to form glomeruli, likely owing to contact-mediated repulsion between axons expressing identical combinations of Pcdh isoforms. |
| Author | Chen, Weisheng V. Mountoufaris, George Chevee, Maxime Nwakeze, Chiamaka L. Maniatis, Tom O’Keeffe, Sean Polleux, Franck Hirabayashi, Yusuke |
| AuthorAffiliation | 1 Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA 2 Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10032, USA 3 Department of Neuroscience, Kavli Institute for Brain Science, Columbia University, New York, NY 10032, USA |
| AuthorAffiliation_xml | – name: 3 Department of Neuroscience, Kavli Institute for Brain Science, Columbia University, New York, NY 10032, USA – name: 1 Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA – name: 2 Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10032, USA |
| Author_xml | – sequence: 1 givenname: George surname: Mountoufaris fullname: Mountoufaris, George – sequence: 2 givenname: Weisheng V. surname: Chen fullname: Chen, Weisheng V. – sequence: 3 givenname: Yusuke surname: Hirabayashi fullname: Hirabayashi, Yusuke – sequence: 4 givenname: Sean surname: O’Keeffe fullname: O’Keeffe, Sean – sequence: 5 givenname: Maxime surname: Chevee fullname: Chevee, Maxime – sequence: 6 givenname: Chiamaka L. surname: Nwakeze fullname: Nwakeze, Chiamaka L. – sequence: 7 givenname: Franck surname: Polleux fullname: Polleux, Franck – sequence: 8 givenname: Tom surname: Maniatis fullname: Maniatis, Tom |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28450637$$D View this record in MEDLINE/PubMed |
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| Snippet | The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters (Pcdhα, Pcdhβ, and Pcdhγ). Here, we show... Neurons in the developing brain cooperate to build circuits. Mountoufaris et al. found that ∼50 variable protocadherin genes support a combinatorial identity... The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters ( α, β, and γ). Here, we show that all... Neurons in the developing brain cooperate to build circuits. Mountoufaris et al. found that ∼50 variable protocadherin genes support a combinatorial identity... Pattern formation in the brain: Neurons in the developing brain cooperate to build circuits. Mountoufaris et al. found that similar to 50 variable... The vertebrate clustered protocadherin (Pcdh) cell surface proteins are encoded by three closely linked gene clusters ( Pcdh α, Pcdh β, and Pcdh γ). Here, we... |
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| SubjectTerms | Anatomy Animals Assembly Avoidance Axons Axons - physiology Brain Cadherins - genetics Cell surface Central nervous system Circuits Clonal deletion Clusters Combinatorial analysis Deletion Gene clusters Gene Deletion Gene Expression Genes Genetic Variation Glomerulus Isoforms Mice Mice, Inbred C57BL Multigene Family Nerve Net - growth & development Nervous system Neurogenesis - genetics Neurons Odorant receptors Olfactory bulb Olfactory glomeruli Olfactory pathways Olfactory receptor neurons Olfactory Receptor Neurons - physiology Proteins Protocadherin Receptors Rodents Sensory neurons Serotonin Vesicular Glutamate Transport Protein 2 - genetics |
| Title | Multicluster Pcdh diversity is required for mouse olfactory neural circuit assembly |
| URI | https://www.jstor.org/stable/26398900 https://www.ncbi.nlm.nih.gov/pubmed/28450637 https://www.proquest.com/docview/1892778655 https://www.proquest.com/docview/1893546442 https://www.proquest.com/docview/1901705756 https://www.proquest.com/docview/1904246055 https://pubmed.ncbi.nlm.nih.gov/PMC5529182 |
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