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The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation.

ABSTRACT: Because microtubules perform many essential functions in neurons, delineating unique roles attributable to these organelles presents a formidable challenge. Microtubules endow neurons with shape and structure and are required for developmental processes including neurite outgrowth, intracellular transport, and synapse formation and plasticity; microtubules in sensory neurons may be required for the above processes in addition to a specific sensory function. In Caenorhabditis elegans, six touch receptor neurons (TRNs) sense gentle touch and uniquely contain 15-protofilament microtubules. Disruption of these microtubules by loss of either the MEC-7 beta-tubulin or MEC-12 alpha-tubulin or by growth in 1 mM colchicine causes touch insensitivity, altered distribution of the touch transduction channel, and a general reduction in protein levels. We show that the effect on touch sensitivity can be separated from the others; microtubule depolymerization in mature TRNs causes touch insensitivity but does not result in protein distribution and production defects. In addition, the mec-12(e1605) mutation selectively causes touch insensitivity without affecting microtubule formation and other cellular processes. Touching e1605 animals produces a reduced mechanoreceptor current that inactivates more rapidly than in wild-type, suggesting a specific role of the microtubules in mechanotransduction.

SUBMITTER: Bounoutas A

PROVIDER: S-EPMC2757273 | biostudies-literature | 2009 Aug

REPOSITORIES: biostudies-literature

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The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation.

Bounoutas Alexander A O'Hagan Robert R Chalfie Martin M

Current biology : CB 20090716 16

Because microtubules perform many essential functions in neurons, delineating unique roles attributable to these organelles presents a formidable challenge. Microtubules endow neurons with shape and structure and are required for developmental processes including neurite outgrowth, intracellular transport, and synapse formation and plasticity; microtubules in sensory neurons may be required for the above processes in addition to a specific sensory function. In Caenorhabditis elegans, six touch r ...[more]

PMID: 19615905

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Project description:Ciliary and flagellar microtubules contain a specialized set of three protofilaments, termed ribbons, that are composed of tubulin and several associated proteins. Previous studies of sea urchin sperm flagella identified three of the ribbon proteins as tektins, which form coiled-coil filaments in doublet microtubules and which are associated with basal bodies and centrioles. To study the function of tektins and other ribbon proteins in the assembly of flagella and basal bodies, we have begun an analysis of ribbons from the unicellular biflagellate, Chlamydomonas reinhardtii, and report here the molecular characterization of the ribbon protein rib43a. Using antibodies against rib43a to screen an expression library, we recovered a full-length cDNA clone that encodes a 42,657-Da polypeptide. On Northern blots, the rib43a cDNA hybridized to a 1. 7-kb transcript, which was up-regulated upon deflagellation, consistent with a role for rib43a in flagellar assembly. The cDNA was used to isolate RIB43a, an approximately 4.6-kb genomic clone containing the complete rib43a coding region, and restriction fragment length polymorphism analysis placed the RIB43a gene on linkage group III. Sequence analysis of the RIB43a gene indicates that the substantially coiled-coil rib43a protein shares a high degree of sequence identity with clones from Trypanosoma cruzi and Homo sapiens (genomic, normal fetal kidney, and endometrial and germ cell tumors) but little sequence similarity to other proteins including tektins. Affinity-purified antibodies against native and bacterially expressed rib43a stained both flagella and basal bodies by immunofluorescence microscopy and stained isolated flagellar ribbons by immuno-electron microscopy. The structure of rib43a and its association with the specialized protofilament ribbons and with basal bodies is relevant to the proposed role of ribbons in forming and stabilizing doublet and triplet microtubules and in organizing their three-dimensional structure.

Dataset Information

The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation.

Publications

The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation.

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