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

Overview

Journal Mol Cells

Publisher Elsevier

Specialties Cell Biology
Molecular Biology

Date 2014 Dec 6

PMID 25475546

Citations 7

Authors

Juyeon Lee

Jaya Bandyopadhyay

Jin Il Lee

Injeong Cho

Daeho Park

Jeong Hoon Cho

Affiliations

Soon will be listed here.

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.

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References

Thacker C, Srayko M, Rose A . Mutational analysis of bli-4/kpc-4 reveals critical residues required for proprotein convertase function in C. elegans. Gene. 2000; 252(1-2):15-25. DOI: 10.1016/s0378-1119(00)00211-0. View

Peterfi Z, Geiszt M . Peroxidasins: novel players in tissue genesis. Trends Biochem Sci. 2014; 39(7):305-7. DOI: 10.1016/j.tibs.2014.05.005. View

Dickson B . Molecular mechanisms of axon guidance. Science. 2002; 298(5600):1959-64. DOI: 10.1126/science.1072165. View

Brenner S . The genetics of Caenorhabditis elegans. Genetics. 1974; 77(1):71-94. PMC: 1213120. DOI: 10.1093/genetics/77.1.71. View

Peters K, McDowall J, Rose A . Mutations in the bli-4 (I) locus of Caenorhabditis elegans disrupt both adult cuticle and early larval development. Genetics. 1991; 129(1):95-102. PMC: 1204585. DOI: 10.1093/genetics/129.1.95. View

Nelson R, Fessler L, Takagi Y, Blumberg B, Keene D, OLSON P . Peroxidasin: a novel enzyme-matrix protein of Drosophila development. EMBO J. 1994; 13(15):3438-47. PMC: 395246. DOI: 10.1002/j.1460-2075.1994.tb06649.x. View

Thacker C, Peters K, Srayko M, Rose A . The bli-4 locus of Caenorhabditis elegans encodes structurally distinct kex2/subtilisin-like endoproteases essential for early development and adult morphology. Genes Dev. 1995; 9(8):956-71. DOI: 10.1101/gad.9.8.956. View

Mello C, Fire A . DNA transformation. Methods Cell Biol. 1995; 48:451-82. View

Tessier-Lavigne M, Goodman C . The molecular biology of axon guidance. Science. 1996; 274(5290):1123-33. DOI: 10.1126/science.274.5290.1123. View

10.

Gupta M, Graham P, Kramer J . 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. 1997; 137(5):1185-96. PMC: 2136222. DOI: 10.1083/jcb.137.5.1185. View

11.

Jin Y, Jorgensen E, Hartwieg E, Horvitz H . The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J Neurosci. 1999; 19(2):539-48. PMC: 6782196. View

12.

Mueller B . Growth cone guidance: first steps towards a deeper understanding. Annu Rev Neurosci. 1999; 22:351-88. DOI: 10.1146/annurev.neuro.22.1.351. View

13.

Knobel K, Jorgensen E, Bastiani M . Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development. 1999; 126(20):4489-98. DOI: 10.1242/dev.126.20.4489. View

14.

Gotenstein J, Swale R, Fukuda T, Wu Z, Giurumescu C, Goncharov A . The C. elegans peroxidasin PXN-2 is essential for embryonic morphogenesis and inhibits adult axon regeneration. Development. 2010; 137(21):3603-13. PMC: 2964093. DOI: 10.1242/dev.049189. View

15.

Topf U, Chiquet-Ehrismann R . 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. 2011; 22(18):3331-43. PMC: 3172259. DOI: 10.1091/mbc.E10-10-0853. View

16.

Weiss S . Peroxidasin: tying the collagen-sulfilimine knot. Nat Chem Biol. 2012; 8(9):740-1. DOI: 10.1038/nchembio.1050. View

17.

Bhave G, Cummings C, Vanacore R, Kumagai-Cresse C, Ero-Tolliver I, Rafi M . Peroxidasin forms sulfilimine chemical bonds using hypohalous acids in tissue genesis. Nat Chem Biol. 2012; 8(9):784-90. PMC: 4128002. DOI: 10.1038/nchembio.1038. View

18.

Soudi M, Zamocky M, Jakopitsch C, Furtmuller P, Obinger C . Molecular evolution, structure, and function of peroxidasins. Chem Biodivers. 2012; 9(9):1776-93. PMC: 3533774. DOI: 10.1002/cbdv.201100438. View

19.

Fidler A, Vanacore R, Chetyrkin S, Pedchenko V, Bhave G, Yin V . A unique covalent bond in basement membrane is a primordial innovation for tissue evolution. Proc Natl Acad Sci U S A. 2013; 111(1):331-6. PMC: 3890831. DOI: 10.1073/pnas.1318499111. View

20.

Peterfi Z, Toth Z, Kovacs H, Lazar E, Sum A, Donko A . Peroxidasin-like protein: a novel peroxidase homologue in the human heart. Cardiovasc Res. 2013; 101(3):393-9. DOI: 10.1093/cvr/cvt256. View