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In vitro proteolysis of nematode FMRFamide-like peptides (FLPs) by preparations from a free-living nematode (Panagrellus redivivus) and two plant-parasitic nematodes (Heteroderaglycines and Meloidogyne incognita)

Published online by Cambridge University Press:  11 March 2011

E.P. Masler
E.P. Masler*
Affiliation:
Nematology Laboratory, United States Department of Agriculture, Agricultural Research Service, 10300 Baltimore Avenue, BARC-West, BeltsvilleMD20705-2350, USA
*
*Fax: +1 301-504-5589 E-mail: edward.masler@ars.usda.gov
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Abstract

Proteolytic activities in extracts from three nematodes, the plant parasites Heterodera glycines and Meloidogyneincognita, and the free-living Panagrellus redivivus, were surveyed for substrate preferences using a battery of seven FRET-modified peptide substrates, all derived from members of the large FMRF-amide like peptide (FLP) family in nematodes. Overall protease activity in P. redivivus was four- to fivefold greater than in either of the parasites, a result that might reflect developmental differences. Digestion of the M. incognita FLP KHEFVRFa (substrate Abz-KHEFVRF-Y(3-NO2)a) by M. incognita extract was sevenfold greater than with H. glycines extract and twofold greater than P. redivivus, suggesting species-specific preferences. Additional species differences were revealed upon screening 12 different protease inhibitors. Two substrates were used in the screen, Abz-KHEFVRF-Y(3-NO2)a and Abz-KPSFVRF-Y(3-NO2)a), which was digested equally by all three species. The effects of various inhibitor, substrate and extract source combinations on substrate digestion suggest that M. incognita differs significantly from P. redivivus and H. glycines in its complement of cysteine proteases, particularly cathepsin L-type protease.

Type
Research Papers
Information
Journal of Helminthology , Volume 86 , Issue 1 , March 2012 , pp. 77 - 84
Copyright
Copyright © Cambridge University Press 2011. This is a work of the U.S. Government and is not subject to copyright protection in the United States.

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References

Barrett, A.J., Kembhavi, A.A., Brown, M.A., Kirschke, H., Knight, C.G., Tamai, M. & Hanada, K. (1982) L-trans-Epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogs as inhibitors of cysteine proteases including cathepsins B, H, and L. Biochemical Journal 201, 189–198.Google Scholar
Chitwood, D.J., Lusby, W.R., Thompson, M.J., Kochansky, J.P. & Howarth, O.W. (1995) The glycosylceramides of the nematode Caenorhabditis elegans contain an unusual, branched chain sphingoid base. Lipids 30, 567–573.CrossRefGoogle ScholarPubMed
Cohen, M., Reale, V., Olofsson, B., Knights, A., Evans, P. & de Bono, M. (2009) Coordinated regulation of foraging and metabolism in C. elegans by RFamide neuropeptide signaling. Cell Metabolism 9, 375–385.CrossRefGoogle Scholar
Greenwood, K., Williams, T. & Geary, T. (2005) Nematode neuropeptide receptors and their development as anthelmintic screens. Parasitology 131, S169–S177.Google Scholar
Husson, S.J., Mertens, I., Janssen, T., Lindemans, M. & Schoofs, L. (2007) Neuropeptidergic signaling in the nematode Caenorhabditis elegans. Progress in Neurobiology 82, 33–55.CrossRefGoogle ScholarPubMed
Johnston, M.J.G., McVeigh, P., McMaster, S., Fleming, C.C. & Maule, A.G. (2010) FMRFamide-like peptides in root knot nematodes and their potential role in nematode physiology. Journal of Helminthology 84, 253–265.CrossRefGoogle ScholarPubMed
Kimber, M.J. & Fleming, C.C. (2005) Neuromuscular function in plant parasitic nematodes: a target for novel control strategies? Parasitology 131, S129–S142.Google Scholar
Kimber, M.J., McKinney, S., McMaster, S., Day, T.A., Fleming, C.C. & Maule, A.G. (2007) flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB Journal 21, 1233–1243.CrossRefGoogle Scholar
Kirschke, H. (2004) Cathepsin L. pp. 1097–1102in Barrett, A.J., Rawlings, N.D. & Woessner, J.F. (Eds) Handbook of proteolytic enzymes, Vol. 2. Cysteine, serine and threonine peptidases. 2nd edn. Amsterdam, Elsevier Academic Press.Google Scholar
Li, C. (2005) The ever-expanding neuropeptide gene families in the nematode Caenorhabditis elegans. Parasitology 131, S109–S127.CrossRefGoogle ScholarPubMed
Liu, T., Kim, K., Li, C. & Barr, M.M. (2007) FMRFamide-like peptides and mechanosensory touch receptor neurons regulate male sexual turning behavior in Caenorhabditis elegans. Journal of Neuroscience 27, 7174–7182.CrossRefGoogle ScholarPubMed
Lunn, G. & Sansone, E.B. (1994) Degradation and disposal of some enzyme inhibitors. Applied Biochemistry and Biotechnology 48, 57–59.CrossRefGoogle ScholarPubMed
Marks, N.J., Shaw, C., Maule, A.G., Davis, J.P., Halton, D.W., Verhaert, P., Geary, T.G. & Thompson, D.P. (1995) Isolation of AF2 (KHEYLRFamide) from Caenorhabditis elegans: evidence for the presence of more than one FMRFamide-related peptide encoding gene. Biochemical and Biophysical Research Communications 217, 845–851.CrossRefGoogle ScholarPubMed
Masler, E.P. (2007) Characterization of aminopeptidase in the free-living nematode Panagrellus redivivus: subcellular distribution and possible role in neuropeptide metabolism. Journal of Nematology 39, 153–160.Google ScholarPubMed
Masler, E.P. (2008) Digestion of invertebrate neuropeptides by preparations from the free-living nematode Panagrellus redivivus. Journal of Helminthology 82, 279–285.CrossRefGoogle ScholarPubMed
Masler, E.P., Kovaleva, E.S. & Sardanelli, S. (2001) Aminopeptidase-like activities in Caenorhabditis elegans and the soybean cyst nematode, Heterodera glycines. Journal of Helminthology 75, 267–272.Google ScholarPubMed
Maule, A.G., Mousley, A., Marks, N.J., Day, T.A., Thompson, D.P., Geary, T.G. & Halton, D.W. (2002) Neuropeptide signaling systems – potential drug targets for parasite control. Current Topics in Medicinal Chemistry 2, 733–758.CrossRefGoogle Scholar
McVeigh, P., Leech, S., Mair, G.R., Marks, N.J., Geary, T.G. & Maule, A.G. (2005) Analysis of FMRFamide-like peptide (FLP) diversity in phylum Nematoda. International Journal for Parasitology 35, 1043–1060.CrossRefGoogle ScholarPubMed
McVeigh, P., Geary, T.G., Marks, N.J. & Maule, A.G. (2006) The FLP-side of nematodes. Trends in Parasitology 22, 385–396.Google Scholar
Moffett, C.L., Beckett, A.M., Mousley, A., Geary, T.G., Marks, N.J., Halton, D.W., Thompson, D.P. & Maule, A.G. (2003) The ovijector of Ascaris suum: multiple response types revealed by Caenorhabditis elegans FMRFamide-related peptides. International Journal for Parasitology 33, 859–876.CrossRefGoogle ScholarPubMed
Neveu, C., Abad, P. & Castagnone-Sereno, P. (2003) Molecular cloning and characterization of an intestinal cathepsin L protease from the plant-parasitic nematode Meloidogyne incognita. Physiological and Molecular Plant Pathology 63, 159–165.CrossRefGoogle Scholar
Papaioannou, S., Marsden, D., Franks, C.J., Walker, R.J. & Holden-Dye, L. (2005) Role of a FMRFamide-like family of neuropeptides in the pharyngeal nervous system of Caenorhabditis elegans. Journal of Neurobiology 65, 304–319.Google Scholar
Rogers, C., Reale, V., Kim, K., Chatwin, H., Li, C., Evans, P. & de Bono, M. (2003) Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nature Neuroscience 6, 1178–1185.Google Scholar
Sardanelli, S. & Kenworthy, W.J. (1997) Soil moisture control and direct seeding for bioassay of Heterodera glycines on soybean. Journal of Nematology 29, 625–634.Google ScholarPubMed
Shingles, J., Lilley, C.J., Atkinson, H.J. & Urwin, P.E. (2007) Meloidogyne incognita: molecular and biochemical characterization of a cathepsin L cysteine protease and the effect on parasitism following RNAi. Experimental Parasitology 115, 114–120.Google Scholar
Urwin, P.E., Lilley, C.J., McPherson, M.J. & Atkinson, H.J. (1997) Characterization of two cDNAs encoding cysteine proteinases from the soybean cyst nematode Heterodera glycines. Parasitology 114, 605–613.Google Scholar