DOI QR코드

DOI QR Code

A Role for Peroxidasin PXN-1 in Aspects of C. elegans Development

  • Lee, Juyeon (Department of Life Science, Gwangju Institute of Science and Technology) ;
  • Bandyopadhyay, Jaya (Department of Biotechnology, West Bengal University of Technology) ;
  • Lee, Jin Il (Division of Biological Science and Technology, College of Science and Technology, Yonsei University) ;
  • Cho, Injeong (Department of Biology Education, College of Education, Chosun University) ;
  • Park, Daeho (Department of Life Science, Gwangju Institute of Science and Technology) ;
  • Cho, Jeong Hoon (Department of Biology Education, College of Education, Chosun University)
  • Received : 2014.07.18
  • Accepted : 2014.10.24
  • Published : 2015.01.31

Abstract

The Caenorhabditis elegans peroxidasins, PXN-1 and PXN-2, are extracellular peroxidases; pxn-2 is involved in muscle-epidermal attachment during embryonic morphogenesis and in specific axon guidance. Here we investigate potential roles of the other homologue of peroxidasin, pxn-1, in C. elegans. A pxn-1 deletion mutant showed high lethality under heat-stress conditions. Using a transcriptional GFP reporter, pxn-1 expression was observed in various tissues including neurons, muscles, and hypodermis. A translational fusion showed that PXN-1::GFP was secreted and localized in extracellular matrix, particularly along body wall muscles and pharyngeal muscles. Various neuronal developmental defects were observed in pxn-1 mutants and in pxn-1 over-expressing animals, including handedness, branching, breakage, tangling, and defasciculation. These results suggest that pxn-1, like other peroxidasins, plays an important role throughout development.

Keywords

References

  1. Bhave, G., Cummings, C.F., Vanacore, R.M., Kumagai-Cresse, C., Ero-Tolliver, I.A., Rafi, M., Kang, J.S., Pedchenko, V., Fessler, L.I., Fessler, J.H., et al. (2012). Peroxidasin forms sulfilimine chemical bonds using hypohalous acids in tissue genesis. Nat. Chem. Biol. 8, 784-790. https://doi.org/10.1038/nchembio.1038
  2. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
  3. Dickson, B.J. (2002). Molecular mechanisms of axon guidance. Science 298, 1959-1964. https://doi.org/10.1126/science.1072165
  4. Fidler, A.L., Vanacore, R.M., Chetyrkin, S.V., Pedchenko, V.K., Bhave, G., Yin, V.P., Stothers, C.L., Rose, K.L., McDonald, W.H., Clark, T.A., et al. (2014). A unique covalent bond in basement membrane is a primordial innovation for tissue evolution. Proc. Natl. Acad. Sci. USA 111, 331-336. https://doi.org/10.1073/pnas.1318499111
  5. Gotenstein, J.R., Swale, R.E., Fukuda, T., Wu, Z., Giurumescu, C.A., Goncharov, A., Jin, Y., and Chisholm, A.D. (2010). The C. elegans peroxidasin PXN-2 is essential for embryonic morphogenesis and inhibits adult axon regeneration. Development 137, 3603-3613. https://doi.org/10.1242/dev.049189
  6. Gupta, M.C., Graham, P.L., and Kramer, J.M. (1997). Characterization of alpha1(IV) collagen mutations in Caenorhabditis elegans and the effects of alpha1 and alpha2(IV) mutations on type IV collagen distribution. J. Cell Biol. 137, 1185-1196. https://doi.org/10.1083/jcb.137.5.1185
  7. Jin, Y., Jorgensen, E., Hartwieg, E., and Horvitz, H.R. (1999). The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J. Neurosci. 19, 539-548.
  8. Knobel, K.M., Jorgensen, E.M., and Bastiani, M.J. (1999). Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development 126, 4489-4498.
  9. Mello, C., and Fire, A. (1995). DNA transformation. Methods Cell Biol. 48, 451-482. https://doi.org/10.1016/S0091-679X(08)61399-0
  10. Mueller, B.K. (1999). Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 22, 351-388. https://doi.org/10.1146/annurev.neuro.22.1.351
  11. Nelson, R.E., Fessler, L.I., Takagi, Y., Blumberg, B., Keene, D.R., Olson, P.F., Parker, C.G., and Fessler, J.H. (1994). Peroxidasin: a novel enzyme-matrix protein of Drosophila development. EMBO J. 13, 3438-3447.
  12. Peterfi, Z., and Geiszt, M. (2014). Peroxidasins: novel players in tissue genesis. Trends Biochem. Sci. 39, 305-307. https://doi.org/10.1016/j.tibs.2014.05.005
  13. Peterfi, Z., Toth, Z.E., Kovacs, H.A., Lazar, E., Sum, A., Donko, A., Sirokmany, G., Shah, A.M., and Geiszt, M. (2014). Peroxidasinlike protein: a novel peroxidase homologue in the human heart. Cardiovasc. Res. 101, 393-399. https://doi.org/10.1093/cvr/cvt256
  14. Peters, K., McDowall, J., and Rose, A.M. (1991). Mutations in the bli-4 (I) locus of Caenorhabditis elegans disrupt both adult cuticle and early larval development. Genetics 129, 95-102.
  15. Poinat, P., De Arcangelis, A., Sookhareea, S., Zhu, X., Hedgecock, E.M., Labouesse, M., and Georges-Labouesse, E. (2002). A conserved interaction between beta1 integrin/PAT-3 and Nckinteracting kinase/MIG-15 that mediates commissural axon navigation in C. elegans. Curr. Biol. 12, 622-631. https://doi.org/10.1016/S0960-9822(02)00764-9
  16. Soudi, M., Zamocky, M., Jakopitsch, C., Furtmuller, P.G., and Obinger, C. (2012). Molecular evolution, structure, and function of peroxidasins. Chem. Biodivers 9, 1776-1793. https://doi.org/10.1002/cbdv.201100438
  17. Tessier-Lavigne, M., and Goodman, C.S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133. https://doi.org/10.1126/science.274.5290.1123
  18. Thacker, C., Peters, K., Srayko, M., and Rose, A.M. (1995). The bli- 4 locus of Caenorhabditis elegans encodes structurally distinct kex2/subtilisin-like endoproteases essential for early development and adult morphology. Genes Dev. 9, 956-971. https://doi.org/10.1101/gad.9.8.956
  19. Thacker, C., Srayko, M., and Rose, A.M. (2000). Mutational analysis of bli-4/kpc-4 reveals critical residues required for proprotein convertase function in C. elegans. Gene 252, 15-25. https://doi.org/10.1016/S0378-1119(00)00211-0
  20. Topf, U., and Chiquet-Ehrismann, R. (2011). Genetic interaction between Caenorhabditis elegans teneurin ten-1 and prolyl 4- hydroxylase phy-1 and their function in collagen IV-mediated basement membrane integrity during late elongation of the embryo. Mol. Biol. Cell 22, 3331-3343. https://doi.org/10.1091/mbc.E10-10-0853
  21. Weiss, S.J. (2012). Peroxidasin: tying the collagen-sulfilimine knot. Nat. Chem. Biol. 8, 740-741. https://doi.org/10.1038/nchembio.1050

Cited by

  1. Hypergravity hinders axonal development of motor neurons inCaenorhabditis elegans vol.4, 2016, https://doi.org/10.7717/peerj.2666
  2. pxn-1 and pxn-2 May Interact Negatively during Neuronal Development and Aging in C. elegans vol.38, pp.8, 2015, https://doi.org/10.14348/molcells.2015.0124
  3. Muscle and epidermal contributions of the structural protein β-spectrin promote hypergravity-induced motor neuron axon defects in C. elegans vol.10, pp.None, 2020, https://doi.org/10.1038/s41598-020-78414-y