The Invertebrate Microtubule-associated Protein PTL-1 Functions in Mechanosensation and Development in Caenorhabditis Elegans

Overview

Journal Dev Genes Evol

Specialty Biology

Date 2008 Sep 23

PMID 18807071

Citations 24

Authors

Patricia Gordon

Lee Hingula

Michelle L Krasny

Jessica L Swienckowski

Nancy J Pokrywka

Kathleen M Raley-Susman

Affiliations

Soon will be listed here.

Abstract

PTL-1, a microtubule-associated protein of the structural MAP2/tau family, is the sole member of this gene family in Caenorhabditis elegans. Sequence analysis of available invertebrate genomes revealed a number of single, putative tau-like genes with high similarity to ptl-1. The ptl-1 gene is expressed in a number of cells, most notably mechanosensory neurons. We examined the role of ptl-1 in C. elegans in adult neurons as well as during development. A ptl-1 knockout strain of worms exhibited an egg-hatching defect, as well as a reduced sensitivity to touch stimuli. In addition, the knockout allele ptl-1(ok621) acts as a dominant enhancer of several temperature-sensitive alleles of mec-7 and mec-12, which code the isoforms of beta-tubulin and alpha-tubulin that together form the unusual 15 protofilament microtubules involved in touch sensation. These results demonstrate for the first time a functional role for this microtubule-associated protein in nematodes and suggest that PTL-1 is involved in mechanosensation as well as some aspect of embryogenesis.

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References

Goedert M, Baur C, Ahringer J, Jakes R, Hasegawa M, Spillantini M . PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J Cell Sci. 1996; 109 ( Pt 11):2661-72. DOI: 10.1242/jcs.109.11.2661. View

Savage C, Hamelin M, Culotti J, Coulson A, Albertson D, Chalfie M . mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev. 1989; 3(6):870-81. DOI: 10.1101/gad.3.6.870. View

Permana S, Hisanaga S, Nagatomo Y, Iida J, Hotani H, Itoh T . Truncation of the projection domain of MAP4 (microtubule-associated protein 4) leads to attenuation of microtubule dynamic instability. Cell Struct Funct. 2005; 29(5-6):147-57. DOI: 10.1247/csf.29.147. View

Ellgaard L, Riek R, Braun D, Herrmann T, Helenius A, Wuthrich K . Three-dimensional structure topology of the calreticulin P-domain based on NMR assignment. FEBS Lett. 2001; 488(1-2):69-73. DOI: 10.1016/s0014-5793(00)02382-6. View

Doerflinger H, Benton R, Shulman J, St Johnston D . The role of PAR-1 in regulating the polarised microtubule cytoskeleton in the Drosophila follicular epithelium. Development. 2003; 130(17):3965-75. DOI: 10.1242/dev.00616. View

Fukushige T, Siddiqui Z, Chou M, Culotti J, Gogonea C, Siddiqui S . MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J Cell Sci. 1999; 112 ( Pt 3):395-403. DOI: 10.1242/jcs.112.3.395. View

von Bergen M, Barghorn S, Li L, Marx A, Biernat J, Mandelkow E . Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local beta-structure. J Biol Chem. 2001; 276(51):48165-74. DOI: 10.1074/jbc.M105196200. View

Sanchez C, Diaz-Nido J, Avila J . Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol. 2000; 61(2):133-68. DOI: 10.1016/s0301-0082(99)00046-5. View

Gu G, Caldwell G, Chalfie M . Genetic interactions affecting touch sensitivity in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1996; 93(13):6577-82. PMC: 39067. DOI: 10.1073/pnas.93.13.6577. View

10.

Cueva J, Mulholland A, Goodman M . Nanoscale organization of the MEC-4 DEG/ENaC sensory mechanotransduction channel in Caenorhabditis elegans touch receptor neurons. J Neurosci. 2007; 27(51):14089-98. PMC: 6673530. DOI: 10.1523/JNEUROSCI.4179-07.2007. View

11.

McDermott J, Aamodt S, Aamodt E . ptl-1, a Caenorhabditis elegans gene whose products are homologous to the tau microtubule-associated proteins. Biochemistry. 1996; 35(29):9415-23. DOI: 10.1021/bi952646n. View

12.

Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, Fang L . High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol. 2007; 5(9):e237. PMC: 1971126. DOI: 10.1371/journal.pbio.0050237. View

13.

Mukrasch M, von Bergen M, Biernat J, Fischer D, Griesinger C, Mandelkow E . The "jaws" of the tau-microtubule interaction. J Biol Chem. 2007; 282(16):12230-9. DOI: 10.1074/jbc.M607159200. View

14.

Chalfie M, Thomson J . Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans. J Cell Biol. 1982; 93(1):15-23. PMC: 2112106. DOI: 10.1083/jcb.93.1.15. View

15.

Goedert M . Tau gene mutations and their effects. Mov Disord. 2005; 20 Suppl 12:S45-52. DOI: 10.1002/mds.20539. View

16.

Buddle M, Eberhardt E, Ciminello L, Levin T, Wing R, DiPasquale K . Microtubule-associated protein 2 (MAP2) associates with the NMDA receptor and is spatially redistributed within rat hippocampal neurons after oxygen-glucose deprivation. Brain Res. 2003; 978(1-2):38-50. DOI: 10.1016/s0006-8993(03)02758-6. View

17.

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

18.

Siddiqui S, Aamodt E, Rastinejad F, Culotti J . Anti-tubulin monoclonal antibodies that bind to specific neurons in Caenorhabditis elegans. J Neurosci. 1989; 9(8):2963-72. PMC: 6569711. View

19.

Chalfie M, Sulston J, White J, Southgate E, Thomson J, Brenner S . The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci. 1985; 5(4):956-64. PMC: 6565008. View

20.

Rolls M, Satoh D, Clyne P, Henner A, Uemura T, Doe C . Polarity and intracellular compartmentalization of Drosophila neurons. Neural Dev. 2007; 2:7. PMC: 1868948. DOI: 10.1186/1749-8104-2-7. View