Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T05:07:23.642Z Has data issue: false hasContentIssue false

Genistein from Flemingia vestita (Fabaceae) enhances NO and its mediator (cGMP) production in a cestode parasite, Raillietina echinobothrida

Published online by Cambridge University Press:  24 April 2007

B. DAS
Affiliation:
Department of Zoology, North Eastern Hill University, Shillong-793022, India
V. TANDON*
Affiliation:
Department of Zoology, North Eastern Hill University, Shillong-793022, India
N. SAHA
Affiliation:
Department of Zoology, North Eastern Hill University, Shillong-793022, India
*
*Corresponding author. Tel: +91 364 2722312. Fax: +91 364 2550300/2722301. E-mail: tandonveena@hotmail.com

Summary

Cyclic GMP (cGMP) is responsible for various cellular functions including signal pathways and it acts as a mediator for nitric oxide (NO). In order to evaluate the anthelmintic efficacy of the plant-derived isoflavones, the crude peel extract of Flemingia vestita and pure genistein were tested with respect to the activity of nitric oxide synthase (NOS), NO efflux and the cGMP concentration in Rallietina echinobothrida, the cestode parasite of domestic fowl. For comparison, the parasites were also treated with genistein (the major isoflavone present in the crude peel extract), sodium nitroprusside (SNP), a known NO donor, and praziquantel (PZQ), the reference drug. At the time of onset of paralysis in the parasite, the activity of NOS showed a significant increase (35–46%) and a 2-fold increase of NO efflux into the incubation medium in the treated worms in comparison to the respective controls. The cGMP concentration in the parasite tissue increased by 46–84% in the treated test worms in comparison to the controls. The results show that the isoflavones, genistein in particular, from the crude peel extract of F. vestita influence the cGMP concentration in the parasite tissue, which plays a major role in the downstream signal pathways.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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

REFERENCES

Best, P. J., Berger, P. B., Miller, V. M. and Lerman, A. (1998). The effect of estrogen replacement therapy on plasma nitric oxide and endothelin-1 levels in postmenopausal women. Annals of Internal Medicine 128, 285288.CrossRefGoogle ScholarPubMed
Blair, K. L., Bennett, J. L. and Pax, R. A. (1993). Serotonin and acetylcholine: further analysis of praziquantel-induced contraction of magnesium-paralysed Schistosoma mansoni. Parasitology 107, 387395.CrossRefGoogle ScholarPubMed
Breer, H. and Shepherd, G. M. (1993). Implications of the NO/cGMP system for olfaction. Trends in Neurosciences 1, 59.CrossRefGoogle Scholar
Browning, D. D., Windes, N. D. and Ye, R. D. (1999). Activation of p38 mitogen-activated protein kinase by lipopolysaccharide in human neutrophils requires nitric oxide-dependent cGMP accumulation. Journal of Biological Chemistry 274, 537542.CrossRefGoogle ScholarPubMed
Collier, J. and Vallance, P. (1989). Second messenger role for NO widens to nervous and immune systems. Trends in Pharmacological Sciences 10, 427431.CrossRefGoogle ScholarPubMed
Cramer, J. P., Nussler, A. K., Ehrhardt, S., Burkhardt, J., Otchwemah, R. N., Zanger, P., Dietz, E., Gellert, S., Bienzle, U. and Mockenhaupt, F. P. (2005). Age-dependent effect of plasma nitric oxide on parasite density in Ghanaian children with severe malaria. Tropical Medicine and International Health 10, 672680.CrossRefGoogle ScholarPubMed
Das, B., Tandon, V. and Saha, N. (2006). Effect of isoflavone from Flemingia vestita (Fabaceae) on the Ca2+ homeostasis in Raillietina echinobothrida, the cestode of domestic fowl. Parasitology International 55, 1721.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S., Lindholm, A. M., Mäntylä, K., Reuter, M., Lundström, C. A. and Terenina, N. (1998). NO news on the flatworm front! Nitric oxide synthase in parasitic and free living flatworms. Hydrobiologia 383, 161166.CrossRefGoogle Scholar
Gustafsson, M. K. S., Lindholm, A. M., Terenina, N. B. and Reuter, M. (1996). NO nerves in tapeworm. NADPH-diaphorase histochemistry in adult Hymenolepis diminuta. Parasitology 113, 559565.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S., Terenina, N. B., Reuter, M. and Movsessian, S. O. (2003). NO nerves and their targets in a tapeworm: an immunocytochemical study of cGMP in Hymenolepis diminuta. Parasitology Research 90, 148152.CrossRefGoogle Scholar
Hobbs, A. J. (1997). Soluble guanylate cyclase: the forgotten sibling. Trends in Pharmacological Sciences 18, 484491.CrossRefGoogle ScholarPubMed
Hofmann, F. (2005). The biology of cyclic GMP-dependent protein kinases. Journal of Biological Chemistry 280, 14.CrossRefGoogle ScholarPubMed
Holzmuller, P., Cavaleyra, M., Moreaux, J., Kovacic, R., Vincendeau, P., Papierok, G. and Lemesre, J. L. (2005). Lymphocytes of dogs immunised with purified excreted-secreted antigens of Leishmania infantum co-incubated with Leishmania infected macrophages produce IFN gamma resulting in nitric oxide-mediated amastigote apoptosis. Veterinary Immunology and Immunopathology 106, 247257.CrossRefGoogle ScholarPubMed
Ignarro, L. J. (1990). Haem-dependent activation of guanylate cyclase and cyclic GMP formation by endogenous nitric oxide: a unique transduction mechanism for transcellular signaling. Pharmacology and Toxicology 67, 17.CrossRefGoogle ScholarPubMed
Ignarro, L. J., Fokoto, J. M., Griscarage, J. M., Rogers, N. E. and Byrns, R. E. (1993). Oxidation of nitric oxide in aqueous solution to nitrite but not nitrate: comparison of enzymatically formed nitric oxide from L-arginine. Proceedings of the National Academy of Sciences, USA 90, 81038107.CrossRefGoogle Scholar
Imthurn, B., Rosselli, M., Jaeger, A. W., Keller, P. J. and Dubey, R. K. (1997). Differential effects of hormone-replacement therapy on endogenous nitric oxide (nitrite/nitrate) levels in postmenopausal women substituted with 17 beta-estradiol valerate and cyproterone acetate or medroxyprogesterone acetate. Journal of Clinical Endocrinology and Metabolism 82, 388394.Google ScholarPubMed
Kar, P. K., Tandon, V. and Saha, N. (2002). Anthelmintic efficacy of Flemingia vestita: genistein-induced effect on the activity of nitric oxide synthase and nitric oxide in the trematode parasite, Fasciolopsis buski. Parasitology International 51, 249257.CrossRefGoogle ScholarPubMed
Kar, P. K., Tandon, V. and Saha, N. (2004). Anthelmintic efficacy of genistein, the active principle of Flemingia vestita (Fabaceae): alterations in the free amino acid pool and ammonia levels in the fluke, Fasciolopsis buski. Parasitology International 53, 287291.CrossRefGoogle ScholarPubMed
Kohn, A. B., Lea, J. M., Moroz, L. L. and Greenberg, R. M. (2006). Schistosoma mansoni: use of a fluorescent indicator to detect nitric oxide and related species in living parasites. Experimental Parasitology 113, 130133.CrossRefGoogle ScholarPubMed
Kohn, A. B., Moroz, L. L., Lea, J. M. and Greenberg, R. M. (2001). Distribution of nitric oxide synthase immunoreactivity in the nervous system and peripheral tissues of Schistosoma mansoni. Parasitology 122, 8792.CrossRefGoogle ScholarPubMed
Lincoln, T. M. and Cornwell, T. L. (1993). Intracellular cyclic GMP receptor proteins. FASEB Journal 7, 328338.CrossRefGoogle ScholarPubMed
Mahmoud, M. S. and Habib, F. S. (2003). Role of nitric oxide in host defence against Hymenolepis nana infection. Journal of the Egyptian Society of Parasitology 33, 485496.Google ScholarPubMed
Moncada, S., Palmer, R. M. and Higgs, E. A. (1989). Biosynthesis of nitric oxide from L-arginine. A pathway for the regulation of cell function and communication. Biochemical Pharmacology 38, 17091715.CrossRefGoogle ScholarPubMed
Moore, R. B. and Kauffman, N. G. (1970). Simultaneous determination of citrulline and urea using diacetylmonoxime. Analytical Biochemistry 33, 263272.CrossRefGoogle ScholarPubMed
Nathan, C. and Xie, Q. (1994). Regulation of biosynthesis of nitric oxide. Journal of Biological Chemistry 269, 1372513728.CrossRefGoogle ScholarPubMed
Nelson, D. L. and Cox, M. M. (2004). Lehninger Principles of Biochemistry. 4th Edn. Freeman, New York.Google Scholar
Onufriev, M. V., Gulyaeva, N. V., Terenina, N. B., Tolstenkov, O. O. and Gustafsson, M. K. (2005). The effect of a nitric oxide donor on the synthesis of cGMP in Hymenolepis diminuta: a radiometric study. Parasitology Research 95, 2224.CrossRefGoogle ScholarPubMed
Pal, P. and Tandon, V. (1998 a). Anthelmintic efficacy of Flemingia vestita (Fabaceae): genistein-induced alterations in the ultrastructure of the tegument in the cestode, Raillietina echinobothrida. Journal of Parasitic Diseases 22, 104109.Google Scholar
Pal, P. and Tandon, V. (1998 b). Anthelmintic efficacy of Flemingia vestita (Fabaceae): genistein-induced alterations in the activity of tegumental enzymes in the cestode, Raillietina echinobothrida. Parasitology International 47, 233243.CrossRefGoogle Scholar
Pal, P. and Tandon, V. (1998 c). Anthelmintic efficacy of Flemingia vestita (Fabaceae): genistein-induced alterations in the esterase activity in the cestode, Raillietina echinobothrida. Journal of Bioscience 23, 2531.CrossRefGoogle Scholar
Pan, W., Quarles, L. D., Song, L. H., Yu, Y. H., Jiao, C., Tang, H. B., Jiang, C. H., Deng, H. W., Li, Y. J., Zhou, H. H. and Xiao, Z. S. (2005). Genistein stimulates the osteoblastic differentiation via NO/cGMP in bone marrow culture. Journal of Cell Biochemistry 94, 307316.CrossRefGoogle ScholarPubMed
Rao, H. S. P. and Reddy, K. S. (1991). Isoflavones from Flemingia vestita. Fitoterapia 63, 458.Google Scholar
Roy, B. and Tandon, V. (1996). Effect of root-tuber extract of Flemingia vestita a leguminous plant, on Artyfechinostomum sufrartyfex and Fasciolopsis buski: an electron microscopy study. Parasitology Research 82, 248252.CrossRefGoogle ScholarPubMed
Salter, M. and Knowles, R. G. (1998). Measurement of NOS activity by conversion of radiolabelled arginine to citrulline using ion-exchange separation. In Nitric Oxide Protocols (ed. Titheradge, M. A.), pp. 6774. Humana Press, New Jersey.Google Scholar
Sarcevic, B., Brookes, V., Martin, T. J., Kemp, B. E. and Robinson, P. J. (1989). Atrial natriuretic peptide-dependent phosphorylation of smooth muscle cell particulate fraction proteins is mediated by cGMP-dependent protein kinase. Journal of Biological Chemistry 264, 2064820654.CrossRefGoogle ScholarPubMed
Schmidt, H. H. H. W., Lohmann, S. M. and Walter, U. (1993). The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochimica et Biophysica Acta 1178, 153175.CrossRefGoogle ScholarPubMed
Sessa, W. C., Pritchart, K., Seyedi, N., Wang, J. and Hintz, T. H. (1994). Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide gene expression. Circulation Research 74, 349353.CrossRefGoogle Scholar
Sheu, F., Lai, H. H. and Yen, G. C. (2001). Suppression effect of soy isoflavons on nitric oxide production in RAW 264.7 macrophages. Journal of Agricultural Food and Chemistry 49, 17671772.CrossRefGoogle ScholarPubMed
Stuehr, D. J. (1999). Mammalian nitric oxide synthases. Biochimica et Biophysica Acta 1411, 217230.CrossRefGoogle ScholarPubMed
Tandon, V. and Das, B. (2007). In vitro testing of anthelmintic efficacy of Flemingia vestita (Fabaceae) on carbohydrate metabolism in Rallietina echinobothrida. Methods (in the Press) doi:10.1016/j.ymeth.2007.01.005.CrossRefGoogle ScholarPubMed
Tandon, V., Kar, P. K. and Saha, N. (2001). NO nerves in trematodes too! NADPH-diaphorase activity in adult Fasciolopsis buski. Parasitology International 50, 157163.CrossRefGoogle ScholarPubMed
Tandon, V., Pal, P. and Saha, N. (1998). Anthelmintic efficacy of Flemingia vestita (Fabaceae): Genistein-induced alterations in the free amino acid pool of the cestode, Raillietina echinobothrida. Journal of Parasitic Diseases 22, 110115.Google Scholar
Tandon, V., Pal, P., Roy, B., Rao, H. S. P. and Reddy, K. S. (1997). In vitro anthelmintic activity of root tuber extract of Flemingia vestita, an indigenous plant in Shillong, India. Parasitology Research 83, 492498.CrossRefGoogle Scholar
Terenina, N. B. and Gustafsson, M. K. S. (2003). Nitric oxide and its target cells in cercaria of Diplostomum chromatophorum: a histochemical and immunocytochemical study. Parasitology Research 89, 199206.CrossRefGoogle ScholarPubMed
Terenina, N. B., Onufriev, M. V., Gulyaeva, N. V., Lindholm, A. M. and Gustafsson, M. K. S. (2000). A radiometric analysis of Nitric oxide synthase activity in Hymenolepis diminuta. Parasitology 120, 9195.CrossRefGoogle ScholarPubMed
Terenina, N. B., Onufriev, M. V., Gulyaeva, N. V., Moiseeva, Y. V. and Gustafsson, M. K. S. (2003). Nitric oxide synthase activity in Fasciola hepatica: A radiometric study. Parasitology 126, 585590.Google ScholarPubMed
Toda, N. (1995). Nitric oxide and the regulation of central arterial tone. In Nitric Oxide in the Nervous System (ed. Vincent, S. R.), pp. 207225. Academic Press, London.CrossRefGoogle Scholar
Tremblay, J., Gerzer, R. and Hamet, P. (1988). Cyclic GMP in cell function. Advances in Second Messenger Phosphoprotein Research 22, 319383.Google ScholarPubMed