γ-Tubulin Distribution in the Neuron: Implications for the Origins of Neuritic Microtubules

Axons and dendrites contain dense microtubule (MT) arrays that are not attached to a traditional MT nucleating structure such as the centrosome. Nevertheless, the MTs within these neurites are highly organized with respect to their polarity, and consist of a regular 13-protofilament lattice, the two...

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Veröffentlicht in:The Journal of cell biology 1992-10, Vol.119 (1), p.171-178
Hauptverfasser: Baas, Peter W., Joshi, Harish C.
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description Axons and dendrites contain dense microtubule (MT) arrays that are not attached to a traditional MT nucleating structure such as the centrosome. Nevertheless, the MTs within these neurites are highly organized with respect to their polarity, and consist of a regular 13-protofilament lattice, the two known characteristics of MTs nucleated at the centrosome. These observations suggest either that axonal and dendritic MTs arise at the centrosome, or that they are nucleated locally, following a redistribution of MT nucleating material from the centrosome during neuronal development. To begin distinguishing between these possibilities, we have determined the distribution of γ-tubulin within cultured sympathetic neurons. γ-tubulin, a newly discovered protein which is specifically localized to the pericentriolar region of nonneuronal cells (Zheng, Y., M. K. Jung, and B. R. Oakley. 1991. Cell. 65:817-823; Stearns, T., L. Evans, and M. Kirschner. 1991. Cell. 65:825-836), has been shown to play a critical role in MT nucleation in vivo (Joshi, H. C., M. J. Palacios, L. McNamara, and D. W. Cleveland. 1992. Nature (Lond.). 356:80-83). Because the γ-tubulin content of individual cells is extremely low, we relied principally on the high degree of resolution and sensitivity afforded by immunoelectron microscopy. Our studies reveal that, like the situation in nonneuronal cells, γ-tubulin is restricted to the pericentriolar region of the neuron. Furthermore, serial reconstruction analyses indicate that the minus ends of MTs in both axons and dendrites are free of γ-tubulin immunoreactivity. The absence of γ-tubulin from the axon was confirmed by immunoblot analyses of pure axonal fractions obtained from explant cultures. The observation that γ-tubulin is restricted to the pericentriolar region of the neuron provides compelling support for the notion that MTs destined for axons and dendrites are nucleated at the centrosome, and subsequently released for translocation into these neurites.
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Nevertheless, the MTs within these neurites are highly organized with respect to their polarity, and consist of a regular 13-protofilament lattice, the two known characteristics of MTs nucleated at the centrosome. These observations suggest either that axonal and dendritic MTs arise at the centrosome, or that they are nucleated locally, following a redistribution of MT nucleating material from the centrosome during neuronal development. To begin distinguishing between these possibilities, we have determined the distribution of γ-tubulin within cultured sympathetic neurons. γ-tubulin, a newly discovered protein which is specifically localized to the pericentriolar region of nonneuronal cells (Zheng, Y., M. K. Jung, and B. R. Oakley. 1991. Cell. 65:817-823; Stearns, T., L. Evans, and M. Kirschner. 1991. Cell. 65:825-836), has been shown to play a critical role in MT nucleation in vivo (Joshi, H. C., M. J. Palacios, L. McNamara, and D. W. Cleveland. 1992. Nature (Lond.). 356:80-83). 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Nevertheless, the MTs within these neurites are highly organized with respect to their polarity, and consist of a regular 13-protofilament lattice, the two known characteristics of MTs nucleated at the centrosome. These observations suggest either that axonal and dendritic MTs arise at the centrosome, or that they are nucleated locally, following a redistribution of MT nucleating material from the centrosome during neuronal development. To begin distinguishing between these possibilities, we have determined the distribution of γ-tubulin within cultured sympathetic neurons. γ-tubulin, a newly discovered protein which is specifically localized to the pericentriolar region of nonneuronal cells (Zheng, Y., M. K. Jung, and B. R. Oakley. 1991. Cell. 65:817-823; Stearns, T., L. Evans, and M. Kirschner. 1991. Cell. 65:825-836), has been shown to play a critical role in MT nucleation in vivo (Joshi, H. C., M. J. Palacios, L. McNamara, and D. W. Cleveland. 1992. Nature (Lond.). 356:80-83). Because the γ-tubulin content of individual cells is extremely low, we relied principally on the high degree of resolution and sensitivity afforded by immunoelectron microscopy. Our studies reveal that, like the situation in nonneuronal cells, γ-tubulin is restricted to the pericentriolar region of the neuron. Furthermore, serial reconstruction analyses indicate that the minus ends of MTs in both axons and dendrites are free of γ-tubulin immunoreactivity. The absence of γ-tubulin from the axon was confirmed by immunoblot analyses of pure axonal fractions obtained from explant cultures. The observation that γ-tubulin is restricted to the pericentriolar region of the neuron provides compelling support for the notion that MTs destined for axons and dendrites are nucleated at the centrosome, and subsequently released for translocation into these neurites.</description><subject>Animals</subject><subject>Antibodies</subject><subject>Axons</subject><subject>Axons - chemistry</subject><subject>Axons - ultrastructure</subject><subject>Biological and medical sciences</subject><subject>Cell structures and functions</subject><subject>Cells</subject><subject>Cells, Cultured</subject><subject>Centrioles - chemistry</subject><subject>Centrosomes</subject><subject>Cytoskeleton, cytoplasm. Intracellular movements</subject><subject>Dendrites</subject><subject>Dendrites - chemistry</subject><subject>Dendrites - ultrastructure</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Immunoblotting</subject><subject>Microscopy, Immunoelectron</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Molecular and cellular biology</subject><subject>Neurites</subject><subject>Neurites - metabolism</subject><subject>Neurons</subject><subject>Neurons - chemistry</subject><subject>Neurons - ultrastructure</subject><subject>Nucleation</subject><subject>Rats</subject><subject>Schwann cells</subject><subject>Tubulin - analysis</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1992</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkctO3DAUhi0Egimw7K5IWaDuMvjYTpywqFTRcpG4bGCHZJ04DniUiQfbQepz9T36TPVcxGV1dPR_-s_lJ-Qr0CnQip_MdDMFqKcwBQlbZAKFoHkFgm6TCaUM8rpgxR75EsKMUiqk4LtkFwomoawm5PHf3_x-bMbeDtkvG6K3zRitG7LUx2eT3ZrRu-E0u5oveqtxKYWsc34l3nn7ZFPvuhVno9XZjdXexaWjCQdkp8M-mMNN3ScP57_vzy7z67uLq7Of17kWdRVzUwghWyawwwbrijW0lB00ogRqkNaAwgjJZJWubAWylrUlbREFZRxrxku-T36sfRdjMzetNkP02KuFt3P0f5RDqz4rg31WT-5VMVbVJWfJ4PvGwLuX0YSo5jZo0_c4GDcGJTlUIFeT8jWYjgzBm-5tCFC1jEOlOFRaVIFKcST-6ONm7_T6_0k_3ugYNPadx0Hb8IYJnl5Dl9i3NTYL0fl3lzL5lIz_B29_njM</recordid><startdate>19921001</startdate><enddate>19921001</enddate><creator>Baas, Peter W.</creator><creator>Joshi, Harish C.</creator><general>Rockefeller University Press</general><general>The Rockefeller University Press</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19921001</creationdate><title>γ-Tubulin Distribution in the Neuron: Implications for the Origins of Neuritic Microtubules</title><author>Baas, Peter W. ; Joshi, Harish C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c498t-e5447d24afaba982b067f1b4610ea091a4e47278119d4a2d2d60daa4023a92363</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1992</creationdate><topic>Animals</topic><topic>Antibodies</topic><topic>Axons</topic><topic>Axons - chemistry</topic><topic>Axons - ultrastructure</topic><topic>Biological and medical sciences</topic><topic>Cell structures and functions</topic><topic>Cells</topic><topic>Cells, Cultured</topic><topic>Centrioles - chemistry</topic><topic>Centrosomes</topic><topic>Cytoskeleton, cytoplasm. Intracellular movements</topic><topic>Dendrites</topic><topic>Dendrites - chemistry</topic><topic>Dendrites - ultrastructure</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Immunoblotting</topic><topic>Microscopy, Immunoelectron</topic><topic>Microtubules</topic><topic>Microtubules - metabolism</topic><topic>Molecular and cellular biology</topic><topic>Neurites</topic><topic>Neurites - metabolism</topic><topic>Neurons</topic><topic>Neurons - chemistry</topic><topic>Neurons - ultrastructure</topic><topic>Nucleation</topic><topic>Rats</topic><topic>Schwann cells</topic><topic>Tubulin - analysis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Baas, Peter W.</creatorcontrib><creatorcontrib>Joshi, Harish C.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Baas, Peter W.</au><au>Joshi, Harish C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>γ-Tubulin Distribution in the Neuron: Implications for the Origins of Neuritic Microtubules</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>1992-10-01</date><risdate>1992</risdate><volume>119</volume><issue>1</issue><spage>171</spage><epage>178</epage><pages>171-178</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><coden>JCLBA3</coden><abstract>Axons and dendrites contain dense microtubule (MT) arrays that are not attached to a traditional MT nucleating structure such as the centrosome. Nevertheless, the MTs within these neurites are highly organized with respect to their polarity, and consist of a regular 13-protofilament lattice, the two known characteristics of MTs nucleated at the centrosome. These observations suggest either that axonal and dendritic MTs arise at the centrosome, or that they are nucleated locally, following a redistribution of MT nucleating material from the centrosome during neuronal development. To begin distinguishing between these possibilities, we have determined the distribution of γ-tubulin within cultured sympathetic neurons. γ-tubulin, a newly discovered protein which is specifically localized to the pericentriolar region of nonneuronal cells (Zheng, Y., M. K. Jung, and B. R. Oakley. 1991. Cell. 65:817-823; Stearns, T., L. Evans, and M. Kirschner. 1991. Cell. 65:825-836), has been shown to play a critical role in MT nucleation in vivo (Joshi, H. C., M. J. Palacios, L. McNamara, and D. W. Cleveland. 1992. Nature (Lond.). 356:80-83). Because the γ-tubulin content of individual cells is extremely low, we relied principally on the high degree of resolution and sensitivity afforded by immunoelectron microscopy. Our studies reveal that, like the situation in nonneuronal cells, γ-tubulin is restricted to the pericentriolar region of the neuron. Furthermore, serial reconstruction analyses indicate that the minus ends of MTs in both axons and dendrites are free of γ-tubulin immunoreactivity. The absence of γ-tubulin from the axon was confirmed by immunoblot analyses of pure axonal fractions obtained from explant cultures. The observation that γ-tubulin is restricted to the pericentriolar region of the neuron provides compelling support for the notion that MTs destined for axons and dendrites are nucleated at the centrosome, and subsequently released for translocation into these neurites.</abstract><cop>New York, NY</cop><pub>Rockefeller University Press</pub><pmid>1527168</pmid><doi>10.1083/jcb.119.1.171</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record>
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source MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection
subjects Animals
Antibodies
Axons
Axons - chemistry
Axons - ultrastructure
Biological and medical sciences
Cell structures and functions
Cells
Cells, Cultured
Centrioles - chemistry
Centrosomes
Cytoskeleton, cytoplasm. Intracellular movements
Dendrites
Dendrites - chemistry
Dendrites - ultrastructure
Fundamental and applied biological sciences. Psychology
Immunoblotting
Microscopy, Immunoelectron
Microtubules
Microtubules - metabolism
Molecular and cellular biology
Neurites
Neurites - metabolism
Neurons
Neurons - chemistry
Neurons - ultrastructure
Nucleation
Rats
Schwann cells
Tubulin - analysis
title γ-Tubulin Distribution in the Neuron: Implications for the Origins of Neuritic Microtubules
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