Hostname: page-component-84b7d79bbc-fnpn6 Total loading time: 0 Render date: 2024-07-26T05:23:55.419Z Has data issue: false hasContentIssue false

Effects of catechin polyphenols and preparations from the plant–parasitic nematode Heterodera glycines on protease activity and behaviour in three nematode species

Published online by Cambridge University Press:  02 May 2013

E.P. Masler*
Affiliation:
Nematology Laboratory United States, Department of Agriculture, Agricultural Research Service, 10300 Baltimore Avenue, BARC-West, BeltsvilleMD20705-2350, USA

Abstract

Protease activities in preparations from the plant-parasitic nematodes Heterodera glycines and Meloidogyneincognita and the free-living nematode Panagrellus redivivus were inhibited by exposure to a series of eight catechin polyphenol analogues, (+)-catechin, ( − )-epicatechin (EC), ( − )-gallocatechin (GC), ( − )-epigallocatechin (EGC), ( − )-catechin gallate (CG), ( − )-gallocatechin gallate (GCG), ( − )-epicatechin gallate (ECG) and ( − )-epigallocatechin gallate (EGCG) (1 mm each), and by a preparation from H. glycines cysts. General protease activity detected with the FRET-peptide substrate QXL520-KSAYMRF-K(5-FAM)a and proteasome chymotrypsin-like (CTL) activity detected with succinyl-LLVY-AMC were each inhibited significantly more (P< 0.05) by the gallated form of the polyphenol than by the corresponding non-gallated form. Species differences in response to inhibition across all analogues were revealed with the CTL substrate, but CG was a consistently potent inhibitor across all three species and with each substrate. A heat-stable component (CE) from H. glycines cysts inhibited M. incognita CTL activity by 92.07 ± 0.68%, significantly less (P< 0.05) in H. glycines (52.86 ± 2.77%), and by only 17.24 ± 0.55% (P< 0.05) in P. redivivus preparations. CTL activity was, however, inhibited more than 60% in all preparations by the proteasome-specific inhibitor MG-132. Hatching of M. incognita infective juveniles exposed to 1 mm CG, ECG, GCG or EGCG was reduced by 83.88 ± 4.26%, 69.98 ± 9.14%, 94.93 ± 1.71% and 87.93 ± 2.89%, respectively, while hatching of H. glycines was reduced less than 25% by each analogue. CE had no effect on nematode hatch, but did cause a 60% reduction in mobility of H. glycines infective juveniles exposed overnight to CE in vitro, which was more (P< 0.05) than the reduction of M. incognita infective juvenile mobility (20%).

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2013. This is a work of the U.S. Government and is not subject to copyright protection in the United States. 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Brunet, S. & Hoste, H. (2006) Monomers of condensed tannins affect the larval exsheathment of parasitic nematodes of ruminants. Journal of Agricultural and Food Chemistry 54, 74817487.Google Scholar
Charlson, D.C. & Tylka, G.L. (2003) Heterodera glycines cyst components and surface disinfestants affect H. glycines hatching. Journal of Nematology 35, 458464.Google Scholar
Chitwood, D.J. (2003) Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest Management Science 59, 748753.CrossRefGoogle ScholarPubMed
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, 567573.CrossRefGoogle ScholarPubMed
Clarke, A.J. (1968) The chemical composition of the cyst wall of the potato cyst-nematode, Heterodera rostochiensis . Biochemical Journal 108, 221224.CrossRefGoogle ScholarPubMed
Curtis, R.H.C., Robinson, A.F. & Perry, R.N. (2009) Hatch and host location. pp. 139162 in Perry, R.N., Moens, M. & Starr, J.L. (Eds) Root-knot nematodes. Wallingford, Oxfordshire UK, CABI.Google Scholar
Dou, Q.P., Landis-Piwowar, K.R., Chen, D., Huo, C., Wan, S.B. & Chan, T.H. (2008) Green tea polyphenols as a natural tumour cell proteasome inhibitor. Inflammopharmacology 16, 208212.Google Scholar
Kaul, R. (1962) Untersuchungen uber einen aus Zysten des Kartoffelnematoden (Heterodera rostochiensis Woll.) isolierten phenolischen Komplex. Nematologica 8, 288292.Google Scholar
Lam, W.H., Kazi, A., Kuhn, D.J., Chow, L.M.C., Chan, A.S.C., Dou, Q.P. & Chan, T.H. (2004) A potential prodrug for a green tea polyphenol proteasome inhibitor: evaluation of the peracetate ester of ( − ) – epigallocatechin gallate [( − ) – EGCG]. Bioorganic and Medicinal Chemistry 12, 55875593.CrossRefGoogle Scholar
Masler, E.P. (2012) In vitro proteolysis of nematode FMRFamide-like peptides (FLPs) by preparations from a free-living nematode (Panagrellus redivivus) and two plant-parasitic nematodes (Heterodera glycines and Meloidogyne incognita). Journal of Helminthology 86, 7784.CrossRefGoogle ScholarPubMed
Masler, E.P. & Rogers, S.T. (2011) Effects of cyst components and low temperature exposure of Heterodera glycines eggs on juvenile hatching in vitro . Nematology 13, 837844.Google Scholar
Molan, A.L., Meagher, L.P., Spencer, P.A. & Sivakumaran, S. (2003) Effect of flavan-3-ols on in vitro egg hatching, larval development and viability of infective larvae of Trichostrongylus colubriformis . International Journal for Parasitology 33, 16911698.Google Scholar
Nam, S., Smith, D.M. & Dou, Q.P. (2001) Ester bond-containing tea polyphenols potently inhibit proteasome activity in vitro and in vivo. Journal of Biological Chemistry 276, 1332213330.Google Scholar
Niblack, T.L., Lambert, K.N. & Tylka, G.N. (2006) A model plant pathogen from the kingdom Animalia: Heterodera glycines, the soybean cyst nematode. Annual Review of Phytopathology 44, 283303.CrossRefGoogle Scholar
Nour, S.M., Lawrence, J.R., Zhu, H., Swerhone, G.D.W., Welsh, M., Welacky, T.W. & Topp, E. (2003) Bacteria associated with cysts of the soybean cyst nematode (Heterodera glycines). Applied and Environmental Microbiology 69, 607615.CrossRefGoogle ScholarPubMed
Okada, T. (1972) Hatching inhibitory factor in the cyst contents of the soybean cyst nematode, Heterodera glycines Ichinohe (Tylenchida: Heteroderidae). Applied Entomology and Zoology 3, 99102.Google Scholar
Okada, T. (1974) Effects of hatching stimulants obtained from the cyst contents of Heterodera species (Tylenchida: Heteroderidae) on the hatching of other species. Applied Entomology and Zoology 9, 4951.CrossRefGoogle Scholar
Perry, R.N. (2002) Hatching. pp. 147169 in Lee, D. (Ed.) The biology of nematodes. New York, NY, USA, Taylor and Francis.CrossRefGoogle Scholar
Pispa, J., Palmen, S., Holmberg, C.I. & Jantti, J. (2008) C. elegans dss-1 is functionally conserved and required for oogenesis and larval growth. BMC Developmental Biology 8, 51.CrossRefGoogle ScholarPubMed
Pridannikov, M.V., Petelina, G.G., Palchuk, M.V., Masler, E.P. & Dzhavakhiya, V.G. (2007) Influence of components of Globodera rostochiensis cysts on the in vitro hatch of second-stage juveniles. Nematology 9, 837844.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, 625634.Google ScholarPubMed
Shepherd, A.M. & Cox, P.M. (1967) Observations on periodicity of hatching of eggs of the potato cyst nematode, Heterodera rostochiensis Wool. Annals of Applied Biology 60, 143150.Google Scholar
Singh, B.N., Shankar, S. & Srivastava, R.K. (2011) Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochemical Pharmacology 82, 18071821.Google Scholar