Advertisement

Development Genes and Evolution

, Volume 218, Issue 10, pp 541–551 | Cite as

The invertebrate microtubule-associated protein PTL-1 functions in mechanosensation and development in Caenorhabditis elegans

  • Patricia Gordon
  • Lee Hingula
  • Michelle L. Krasny
  • Jessica L. Swienckowski
  • Nancy J. Pokrywka
  • Kathleen M. Raley-SusmanEmail author
Original Article

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 β-tubulin and α-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.

Keywords

Microtubule-associated protein Tau Caenorhabditis elegans Tubulin Neuron 

Notes

Acknowledgments

This work was supported by internal grant awards from the Dean of the Faculty Research Fund, the Abbey Fund and an NIH-AREA award 1R15NS057808-01(to K.M.R.-S.).

We would like to thank Cristian Opazo, Richard Wing, Amory Meltzer, Tasnim Rahman and Charlene Scotland for helpful assistance and Jerry Calvin for assistance with the confocal microscope. We would also like to thank Martin Chalfie for helpful discussions. This paper is dedicated to the memory of Michele Buddle (1962–2004).

References

  1. Altun ZF, Hall DH WormAtlas (2002–2006) http://www.wormatlas.org/ Cited 5 May 2008
  2. Buddle M, Eberhardt E, Ciminello LH, Levin T, Wing R, DiPasquale K, Raley-Susman KM (2003) Microtubule-associated protein 2 (MAP2) associates with the NMDA receptor and is spatially redistributed within rat hippocampal neurons after oxygen–glucose deprivation. Brain Res 978:38–50PubMedCrossRefGoogle Scholar
  3. Chalfie M, Thomson JN (1982) Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans. J Cell Biol 93:15–23PubMedCrossRefGoogle Scholar
  4. Chalfie M, Sulston J, White JG, Southgate E, Thomson JN, Brenner S (1985) The neural circuit for touch sensitivity in C. elegans. J Neurosci 5:956–964PubMedGoogle Scholar
  5. Chen J, Kanai Y, Cowan NJ, Hirokawa N (1992) Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360:674–677PubMedCrossRefGoogle Scholar
  6. Cueva JG, Mulholland A, Goodman MB (2007) Nanoscale organization of the MEC-4/DEG/ENaC sensory mechanotransduction channel in Caenorhabditis elegans touch receptor neurons. J Neurosci 27:14089–14098PubMedCrossRefGoogle Scholar
  7. de Bono M, Maricq AV (2005) Neuronal substrates of complex behaviors in C. elegans. Ann Rev Neurosci 28:451–501PubMedCrossRefGoogle Scholar
  8. Dehmelt L, Halpain S (2004) Actin and microtubules in neurite initiation: are MAPs the missing link? J Neurobio 58:18–33CrossRefGoogle Scholar
  9. Doerflinger H, Benton R, Shulman JM, St.Johnson D (2003) The role of PAR-1 in regulating the polarized microtubule cytoskeleton in the Drosophila follicular epithelium. Dev 130:3967–3975CrossRefGoogle Scholar
  10. Duerr JS (2006) Immunohistochemistry In: WormBook (ed). The C. elegans Research Community, doi: 10.1895/wormbook.1.105.1, http://www.wormbook.org
  11. Ellgaard L, Riek R, Braun D, Herrmann T, Helenius A, Wuthrich K (2001) Three-dimensional structure topology of the calreticulin P-domain based on NMR assignment. FEBS Lett 488:69–73PubMedCrossRefGoogle Scholar
  12. Ernstrom GG, Chalfie M (2002) Genetics of sensory mechanotransduction. Ann Rev Genetics 36:411–453CrossRefGoogle Scholar
  13. Fukushige T, Siddiqui ZK, Chou M, Culotti JG, Gogonea CB, Siddiqui SS, Hamelin M (1999) MEC-12, an a-tubulin required for touch sensitivity in C. elegans. J Cell Sci 112:395–403PubMedGoogle Scholar
  14. Goedert M (2005) Tau gene mutations and their effects. Movement Disorders 20:S45–S52PubMedCrossRefGoogle Scholar
  15. Goedert M, Baur CP, Ahringer J, Jakes R, Hasegawa M, Spillantini MG, Smith MJ, Hill F (1996) PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J Cell Sci 109:2661–2672PubMedGoogle Scholar
  16. Gu G, Caldwell GA, Chalfie M (1996) Genetic interactions affecting touch sensitivity in Caenorhabditis elegans. Proc Nat Acad Sci 93:6577–6582PubMedCrossRefGoogle Scholar
  17. Hahn M, Borisova S, Schrag JD, Tessier DC, Zapun A, Tom R, Kamen AA, Bergeron JJ, Thomas DY, Cygler M (1998) Identification and crystallization of a protease-resistant core of calnexin that retains biological activity. J Struct Biol 123:260–264PubMedCrossRefGoogle Scholar
  18. Harris TW, Chen N, Cunningham F, Tello-Ruiz M, Antoshechkin I, Bastiani C, Bieri T, Blasiar D, Bradnam K, Chan J, Chen C, Chen WJ, Davis P, Kenny E, Kishore R, Lawson D, Lee R, Muller H, Nakamura C, Ozersky P, Petcherski A, Rogers A, Sabo A, Schwarz EM, Van Auken K, Wang Q, Durbin R, Spieth J, Sternberg PW, Stein LD (2004) WormBase: a multi-species resource for nematode biology and genomics. Nucleic Acids Res 32:D411–D417PubMedCrossRefGoogle Scholar
  19. Hasegawa M, Smith MR, Goedert M (1998) Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett 437:207–210PubMedCrossRefGoogle Scholar
  20. Heidary G, Fortini ME (2001) Identification and characterization of the Drosophila tau homolog. Mech Dev 108:171–178PubMedCrossRefGoogle Scholar
  21. Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, Fang L, Halfnight E, Lee D, Lin J, Lorch A, McKay S, Okada HM (2007) High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLOS Biol 5:1981–1997CrossRefGoogle Scholar
  22. McDermott JB, Aamodt S, Aamodt E (1996) ptl-1, a Caenorhabditis elegans gene whose products are homologous to the tau microtubule-associated proteins. Biochem 35:9415–9423CrossRefGoogle Scholar
  23. McKay SJ, Johnsen R, Khattra J, Asano J, Baillie DL, Chan S, Dube N, Fang L, Goszczynski B, Ha E, Halfnight E (2004) Gene expression profiling of cells, tissues, and developmental stages of the nematode C. elegans. Cold Spring Harbor Symp Quant Biol 68:159–169CrossRefGoogle Scholar
  24. Mukrasch MD, von Bergen M, Biernat J, Fishcher D, Griesinger C, Mandelkow E, Zweckstetter M (2007) The “Jaws” of the tau–microtubule interaction. J Biol Chem 282:12230–12239PubMedCrossRefGoogle Scholar
  25. O'Hagan R, Chalfie M, Goodman MB (2005) The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat Neurosci 8:43–50PubMedCrossRefGoogle Scholar
  26. Permana S, Hisanage S, Nagatomo Y, Iida J, Hotani H, Itoh TJ (2005) Truncation of the projection domain of MAP4 (microtubule-associated protein) leads to attenuation of microtubule dynamic instability. Cell Struct Function 29:147–157CrossRefGoogle Scholar
  27. Riddle DL, Blumenthal T, Meyer BJ, Priess JR (1997) C. elegans II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  28. Rolls MM, Satoh D, Clyne PJ, Henner AL, Uemura T, Doe CQ (2007) Polarity and intracellular compartmentalization of Drosophila neurons. Neural Dev 2:7CrossRefPubMedGoogle Scholar
  29. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  30. Sanchez C, Diaz-Nido J, Avila J (2000) Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobio 61:133–168CrossRefGoogle Scholar
  31. Savage C, Hamelin M, Culotti JG, Coulson A, Albertson DG, Chalfie M (1989) mec-7 is a β-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev 3:870–881PubMedCrossRefGoogle Scholar
  32. Savage C, Xue Y, Mitani S, Hall D, Zakhay R, Chalfie M (1994) Mutations in the Caenorhabditis elegans β-tubulin gene mec-7: effects on microtubule assembly and stability and on tubulin autoregulation. J Cell Sci 107:2165–2175PubMedGoogle Scholar
  33. Siddiqui SS, Aamodt E, Rastinejad F, Culotti JG (1989) Anti-tubulin antibodies that bind to specific neurons in Caenorhabditis elegans. J Neurosci 9:2963–2972PubMedGoogle Scholar
  34. Thierry-Mieg D, Thierry-Mieg J (2006) AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Bio 7:S12CrossRefGoogle Scholar
  35. von Bergen M, Barghorn S, Li L, Marx A, Biernat J, Mandelkow EM, Mandelkow E (2001) Mutations of tau protein in fronto-temporal dementia promote aggregation of paired helical filaments by enhancing local β-structure. J Biol Chem 276:48165–48174Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Patricia Gordon
    • 1
  • Lee Hingula
    • 1
  • Michelle L. Krasny
    • 1
  • Jessica L. Swienckowski
    • 1
  • Nancy J. Pokrywka
    • 1
  • Kathleen M. Raley-Susman
    • 1
    Email author
  1. 1.Department of BiologyVassar CollegePoughkeepsieUSA

Personalised recommendations