Title: 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 [1Gordon-Weeks P.R. Microtubules and growth cone function.J. Neurobiol. 2004; 58: 70-83Crossref PubMed Scopus (170) Google Scholar], intracellular transport [2Goldstein L.S. Yang Z. Microtubule-based transport systems in neurons: The roles of kinesins and dyneins.Annu. Rev. Neurosci. 2000; 23: 39-71Crossref PubMed Scopus (456) Google Scholar], and synapse formation and plasticity [3Chang Q. Balice-Gordon R.J. highwire, rpm-1, and futsch: Balancing synaptic growth and stability.Neuron. 2000; 26: 287-290Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar, 4Bianchi M. Hagan J.J. Heidbreder C.A. Neuronal plasticity, stress and depression: Involvement of the cytoskeletal microtubular system?.Curr. Drug Target. CNS Neurol. Disord. 2005; 4: 597-611Crossref PubMed Scopus (59) Google Scholar]; 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 [5Chalfie M. Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans.Dev. Biol. 1981; 82: 358-370Crossref PubMed Scopus (497) Google Scholar] and uniquely contain 15-protofilament microtubules [6Chalfie M. Thomson J.N. Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans.J. Cell Biol. 1982; 93: 15-23Crossref PubMed Scopus (168) Google Scholar]. Disruption of these microtubules by loss of either the MEC-7 β-tubulin [7Savage C. Hamelin M. Culotti J.G. Coulson A. Albertson D.G. Chalfie M. mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans.Genes Dev. 1989; 3: 870-881Crossref PubMed Scopus (232) Google Scholar] or MEC-12 α-tubulin [8Fukushige T. Siddiqui Z.K. Chou M. Culotti J.G. Gogonea C.B. Siddiqui S.S. Hamelin M. MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans.J. Cell Sci. 1999; 112: 395-403PubMed Google Scholar] or by growth in 1 mM colchicine causes touch insensitivity [5Chalfie M. Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans.Dev. Biol. 1981; 82: 358-370Crossref PubMed Scopus (497) Google Scholar, 6Chalfie M. Thomson J.N. Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans.J. Cell Biol. 1982; 93: 15-23Crossref PubMed Scopus (168) Google Scholar], 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.