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Modulation of murine intestinal immunity by Moringa oleifera extract in experimental hymenolepiasis nana

Published online by Cambridge University Press:  06 April 2017

M. Abdel-Latif*
Affiliation:
Department of Zoology, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt
G. El-Shahawi
Affiliation:
Department of Zoology, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt
S.M. Aboelhadid
Affiliation:
Department of Veterinary Parasitology, Faculty of Veterinary Medicine, Beni-Suef University, Beni-Suef, Egypt
H. Abdel-Tawab
Affiliation:
Department of Zoology, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt

Abstract

The potential therapeutic value of Moringa oleifera extract (MOE), due to its anti-inflammatory and anti-oxidant effects, has been reported previously. In this study, Hymenolepis nana antigen (HNA) in combination with MOE was used in immunization against H. nana infection. Adult worm and egg counts were taken, while histological changes in the intestine were observed. Mucosal mast (MMCs) and goblet cells (GCs) were stained with specific stains, while serum and intestinal IgA were assayed using enzyme-linked immunosorbent assay (ELISA). Reduced glutathione (GSH) and lipid peroxidation (thiobarbituric acid reactive substances, TBARS) were assayed. Real-time polymerase chain reaction (PCR) was used for detection of mRNA expression in ileum tissue. The results demonstrated an improvement in the architecture of intestinal villi, decreased inducible nitric oxide synthase (iNOs) and TBARS, and increased GSH in HNA, MOE and MOE + HNA groups. In the same groups, an increase in GCs, mucin 2 (MUC2), interleukins (IL)-4, -5 and -9, and stem cell factor (SCF) versus a decrease in both interferon-gamma (IFN-γ) and transforming growth factor (TGF-β) expression appeared. HNA and MOE + HNA increased serum and intestinal IgA, respectively. MOE decreased MMCs and achieved the highest reductions in both adult worms and eggs. In conclusion, MOE could achieve protection against H. nana infections through decreased TGF-β, IFN-γ and MMC counts versus increased GC counts, T-helper cell type 2 (Th2) cytokines and IgA level.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

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References

Abdel-Latif, M., Abdel-Haleem, H.M. & Abdel-Baki, A.A. (2016) Anticoccidial activities of chitosan on Eimeria papillata-infected mice. Parasitology Research 115, 28452852.Google Scholar
Abdi, M., Nibret, E. & Munshea, A. (2016) Prevalence of intestinal helminthic infections and malnutrition among schoolchildren of the Zegie Peninsula, northwestern Ethiopia. Journal of Infection and Public Health 10, 8492.Google Scholar
Adams, G.G. & Dilly, P.N. (1989) Differential staining of ocular goblet cells. Eye 3, 840844.Google Scholar
Adedapo, A.A., Falayi, O.O. & Oyagbemi, A.A. (2015) Evaluation of the analgesic, anti-inflammatory, anti-oxidant, phytochemical and toxicological properties of the methanolic leaf extract of commercially processed Moringa oleifera in some laboratory animals. Journal of Basic and Clinical Physiology and Pharmacology 26, 491499.Google Scholar
Ahmed, R.G., Abdel-Latif, M. & Ahmed, F. (2015) Protective effects of GM-CSF in experimental neonatal hypothyroidism. International Immunopharmacology 29, 538543.Google Scholar
Allen, A., Hutton, D.A., Leonard, A.J., Pearson, J.P. & Sellers, L.A. (1986) The role of mucus in the protection of the gastroduodenal mucosa. Scandinavian Journal of Gastroenterology Supplement 125, 7178.Google Scholar
Artis, D. (2006) New weapons in the war on worms: identification of putative mechanisms of immune-mediated expulsion of gastrointestinal nematodes. International Journal for Parasitology 36, 723733.Google Scholar
Bancroft, G.D. & Gamble, M. (2008) Theory and practice of histological techniques. 6th edn. New York, Churchill Livingstone.Google Scholar
Banji, O.J., Banji, D. & Kavitha, R. (2012) Immunomodulatory effects of alcoholic and hydroalcoholic extracts of Moringa oleifera Lam. leaves. Indian Journal of Experimental Biology 50, 270276.Google Scholar
Bortoletti, G., Gabriele, F. & Palmas, C. (1989) Kinetics of mast cells, eosinophils and phospholipase B activity in the spontaneous-cure response of two strains of mice (rapid and slow responder) to the cestode Hymenolepis nana . Parasitology Research 75, 465469.CrossRefGoogle Scholar
Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Caughey, G.H., Viro, N.F., Calonico, L.D., McDonald, D.M., Lazarus, S.C. & Gold, W.M. (1988) Chymase and tryptase in dog mastocytoma cells: asynchronous expression as revealed by enzyme cytochemical staining. Journal of Histochemistry and Cytochemistry 36, 10531060.Google Scholar
Chuang, P.H., Lee, C.W., Chou, J.Y., Murugan, M., Shieh, B.J. & Chen, H.M. (2007) Anti-fungal activity of crude extracts and essential oil of Moringa oleifera Lam. Bioresource Technology 98, 232236.Google Scholar
Coles, G.C., Bauer, C., Borgsteede, F.H., Geerts, S., Klei, T.R., Taylor, M.A. & Waller, P.J. (1992) World Association for the Advancement of Veterinary Parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 44, 3544.Google Scholar
Conchedda, M., Bortoletti, G., Gabriele, F., Wakelin, D. & Palmas, C. (1997) Immune response to the cestode Hymenolepis nana: cytokine production during infection with eggs or cysts. International Journal for Parasitology 27, 321327.CrossRefGoogle ScholarPubMed
Czeczot, H., Skrzycki, M., Majewska-Wierzbicka, M., Podsiad, M., Salamatin, R. & Grytner-Ziecina, B. (2013) The antioxidant defence mechanisms of parasite and host after chronic Hymenolepis diminuta infestation of the rat. Polish Journal of Veterinary Science 16, 121123.Google Scholar
Delic, D., Gailus, N., Vohr, H.W., Dkhil, M., Al-Quraishy, S. & Wunderlich, F. (2010) Testosterone-induced permanent changes of hepatic gene expression in female mice sustained during Plasmodium chabaudi malaria infection. Journal of Molecular Endocrinology 45, 379390.Google Scholar
Ellman, G.L. (1959) Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82, 7077.Google Scholar
Fard, M.T., Arulselvan, P., Karthivashan, G., Adam, S.K. & Fakurazi, S. (2015) Bioactive extract from Moringa oleifera inhibits the pro-inflammatory mediators in lipopolysaccharide stimulated macrophages. Pharmacognosy Magazine 11, 556563.Google Scholar
Featherston, D.W., Wakelin, D. & Lammas, D.A. (1992) Inflammatory responses in the intestine during tapeworm infections. Mucosal mast cells and mucosal mast cell proteases in Sprague–Dawley rats infected with Hymenolepis diminuta . International Journal for Parasitology 22, 961966.CrossRefGoogle ScholarPubMed
Ferreira, P.M.P., Farias, D.F., Oliveira, J.T.A. & Carvalho, A.F.U. (2008) Moringa oleifera: bioactive compounds and nutritional potential. Revista de Nutrição 21, 431437.Google Scholar
Finkelman, F.D., Shea-Donohue, T., Goldhill, J., Sullivan, C.A., Morris, S.C., Madden, K.B., Gause, W.C. & Urban, J.F. Jr (1997) Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annual Review of Immunology 15, 505533.Google Scholar
Fonseca-Coronado, S., Ruiz-Tovar, K., Pérez-Tapia, M., Mendlovic, F. & Flisser, A. (2011) Taenia solium: immune response against oral or systemic immunization with purified recombinant calreticulin in mice. Experimental Parasitology 127, 313317.Google Scholar
Gabriele, F., Ecca, A.R., Aru, A.B. & Palmas, C. (1985) Vaccination against the gastrointestinal helminthes Trichinella spiralis and Hymenolepis nana: relationship between routes of immunization and effective protection. Bollettino dell'Istituto Sieroterapico Milanese 64, 408413.Google Scholar
Gebhardt, T., Lorentz, A., Detmer, F., Trautwein, C., Bektas, H., Manns, M.P. & Bischoff, S.C. (2005) Growth, phenotype, and function of human intestinal mast cells are tightly regulated by transforming growth factor beta1. Gut 54, 928934.CrossRefGoogle ScholarPubMed
Gounaris, E., Erdman, S.E., Restaino, C., Gurish, M.F., Friend, D.S., Gounari, F., Lee, D.M., Zhang, G., Glickman, J.N., Shin, K., Rao, V.P., Poutahidis, T., Weissleder, R., McNagny, K.M. & Khazaie, K. (2007) Mast cells are an essential hematopoietic component for polyp development. Proceedings of the National Academy of Sciences of the United States of America 104, 1997719982.CrossRefGoogle ScholarPubMed
Hayes, K.S., Bancroft, A.J. & Grencis, R.K. (2004) Immune-mediated regulation of chronic intestinal nematode infection. Immunological Reviews 201, 7588.CrossRefGoogle ScholarPubMed
Henderson, D. & Hanna, R. (1987) Hymenolepis nana (Cestoda: Cyclophyllidea): migration, growth and development in the laboratory mouse. International Journal for Parasitology 17, 12491256.CrossRefGoogle ScholarPubMed
Ishih, A. & Uchikawa, R. (2000) Immunoglobulin E and mast cell responses are related to worm biomass but not expulsion of Hymenolepis diminuta during low dose infection in rats. Parasite Immunology 22, 561566.Google Scholar
Ishikawa, N., Horii, Y. & Nawa, Y. (1993) Immune-mediated alteration of the terminal sugars of goblet cell mucins in the small intestine of Nippostrongylus brasiliensis-infected rats. Immunology 78, 303307.Google Scholar
Ishiwata, K. & Watanabe, N. (2007) Nippostrongylus brasiliensis: reversibility of reduced-energy status associated with the course of expulsion from the small intestine in rats. Experimental Parasitology 117, 8086.CrossRefGoogle ScholarPubMed
Ito, A., Onitake, K., Sasaki, J. & Takami, T. (1991) Hymenolepis nana: immunity against oncosphere challenge in mice previously given viable or non-viable oncospheres of H. nana, H. diminuta, H. microstoma and Taenia taeniaeformis . International Journal for Parasitology 21, 241245.CrossRefGoogle ScholarPubMed
Kaneko, M., Akiyama, Y., Takimoto, H. & Kumazawa, Y. (2005) Mechanism of up-regulation of immunoglobulin A production in the intestine of mice unresponsive to lipopolysaccharide. Immunology 116, 6470.CrossRefGoogle ScholarPubMed
Khan, W.I. & Collins, S.M. (2004) Immune-mediated alteration in gut physiology and its role in host defence in nematode infection. Parasite Immunology 26, 319326.Google Scholar
Kifleyohannes, T., Terefe, G., Tolossa, Y.H., Giday, M. & Kebede, N. (2014) Effect of crude extracts of Moringa stenopetala and Artemisia absinthium on parasitaemia of mice infected with Trypanosoma congolense . BMC Research Notes 7, 390.Google Scholar
Kurokawa, M., Wadhwani, A., Kai, H., Hidaka, M., Yoshida, H., Sugita, C., Watanabe, W., Matsuno, K. & Hagiwara, A. (2016) Activation of cellular immunity in herpes simplex virus type 1-infected mice by the oral administration of aqueous extract of Moringa oleifera Lam. leaves. Phytotherapy Research 30, 797804.Google Scholar
Leder, L.D. (1979) The chloroacetate esterase reaction: a useful means of histological diagnosis of hematological disorders from paraffin sections of skin. American Journal of Dermatopathology 1, 3942.Google Scholar
Lee, H.J., Jeong, Y.J., Lee, T.S., Park, Y.Y., Chae, W.G., Chung, I.K., Chang, H.W., Kim, C.H., Choi, Y.H., Kim, W.J., Moon, S.K. & Chang, Y.C. (2013) Moringa fruit inhibits LPS-induced NO/iNOS expression through suppressing the NF-κB activation in RAW264.7 cells. American Journal of Chinese Medicine 41, 11091123.Google Scholar
Leone, A., Spada, A., Battezzati, A., Schiraldi, A., Aristil, J. & Bertoli, S. (2015) Cultivation, genetic, ethnopharmacology, phytochemistry and pharmacology of Moringa oleifera leaves: an overview. International Journal of Molecular Sciences 16, 1279112835.CrossRefGoogle ScholarPubMed
Levecke, B., Behnke, J.M., Ajjampur, S.S., Albonico, M., Ame, S.M., Charlier, J., Geiger, S.M., Hoa, N.T., KamwaNgassam, R.I., Kotze, A.C., McCarthy, J.S., Montresor, A., Periago, M.V., Roy, S., TchuemTchuenté, L.A., Thach, D.T. & Vercruysse, J. (2011) A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato–Katz thick smear methods for soil-transmitted helminths. PLoS Neglected Tropical Diseases 5, e1201.Google Scholar
Lorentz, A., Wilke, M., Sellge, G., Worthmann, H., Klempnauer, J., Manns, M.P. & Bischoff, S.C. (2005) IL-4-induced priming of human intestinal mast cells for enhanced survival and Th2 cytokine generation is reversible and associated with increased activity of ERK1/2 and c-Fos. Journal Immunology 174, 67516756.Google Scholar
Maggini, S., Wintergerst, E.S., Beveridge, S. & Hornig, D.H. (2007) Selected vitamins and trace elements support immune function by strengthening epithelial barriers and cellular and humoral immune responses. British Journal of Nutrition 98, 2935.CrossRefGoogle ScholarPubMed
Matsuzawa, K., Abe, M., Shirakura, T., Zhao, W.H. & Nakamura, F. (2008) Spontaneous worm expulsion and intestinal IgA response in mice infected by Vampirolepis nana . Parasitology International 57, 512514.Google Scholar
McLauchlan, P.E., Roberts, H.C., Loxton, N.J., Wastling, J.M., Newlands, G.F. & Chappell, L.H. (1999) Mucosal mast cell responses and release of mast cell protease-I in infections of mice with Hymenolepis diminuta and H. microstoma: modulation by cyclosporin A. Parasite Immunology 21, 151161.Google Scholar
Mekonnen, Y., Yardley, V., Rock, P. & Croft, S. (1999) In vitro antitrypanosomal activity of Moringa stenopetala leaves and roots. Phytotherapy Research 13, 538539.Google Scholar
Morimoto, M. (2011) Intestinal smooth muscle cells locally enhance stem cell factor (SCF) production against gastrointestinal nematode infections. Journal of Veterinary Medical Science 73, 805807.Google Scholar
Murray, P.D., Foster, W.B. & Passmore, H.C. (1984) Hymenolepis microstoma: mouse strain differences in resistance to a challenge infection. Experimental Parasitology 58, 325332.CrossRefGoogle ScholarPubMed
Nfambi, J., Bbosa, G.S., Sembajwe, L.F., Gakunga, J. & Kasolo, J.N. (2015) Immunomodulatory activity of methanolic leaf extract of Moringa oleifera in Wistar albino rats. Journal of Basic Clinical Physiology and Pharmacology 26, 603611.Google Scholar
Ohkawa, H., Ohishi, N. & Yagi, K. (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95, 351358.Google Scholar
Ola-Fadunsin, S.D. & Ademola, I.O. (2013) Direct effects of Moringa oleifera Lam. (Moringaceae) acetone leaf extract on broiler chickens naturally infected with Eimeria species. Tropical Animal Health and Production 45, 14231428.Google Scholar
Ovington, K.S., McKie, K., Matthaei, K.I., Young, I.G. & Behm, C.A. (1998) Regulation of primary Strongyloides ratti infections in mice: a role for interleukin-5. Immunology 95, 488493.Google Scholar
Pemberton, A.D., Brown, J.K., Wright, S.H., Knight, P.A. & Miller, H.R. (2006) The proteome of mouse mucosal mast cell homologues: the role of transforming growth factor beta1. Proteomics 6, 623631.Google Scholar
Persaud, R., Wang, A., Reardon, C. & McKay, D.M. (2007) Characterization of the immuno-regulatory response to the tapeworm Hymenolepis diminuta in the non-permissive mouse host. International Journal for Parasitology 37, 393403.Google Scholar
Rostami, A., Ebrahimi, M., Mehravar, S., Fallah Omrani, V., Fallahi, S. & Behniafar, H. (2016) Contamination of commonly consumed raw vegetables with soil transmitted helminth eggs in Mazandaran province, northern Iran. International Journal of Food Microbiology 225, 5458.Google Scholar
Salles, H.O., Braga, A.C., Nascimento, M.T., Sousa, A.M., Lima, A.R., Vieira Lda, S., Cavalcante, A.C., Egito, A.S. & Andrade, L.B. (2014) Lectin, hemolysin and protease inhibitors in seed fractions with ovicidal activity against Haemonchus contortus . Revista Brasileira de Parasitologia Veterinária 23, 136143.Google Scholar
Sanad, M.M. & Al-Furaeihi, L.M. (2006) Effect of some immunomodulators on the host–parasite system in experimental Hymenolepiasis nana . Journal of Egypt Society of Parasitology 36, 6580.Google Scholar
Sedlak, J. & Lindsay, R.H. (1968) Estimation of total, protein bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Analytical Biochemistry 25, 192205.Google Scholar
Sellge, G., Barkowsky, M., Kramer, S., Gebhardt, T., Sander, L.E., Lorentz, A. & Bischoff, S.C. (2014) Interferon-γ regulates growth and controls Fcγ receptor expression and activation in human intestinal mast cells. BMC Immunology 15, 27.Google Scholar
Shekels, L.L., Anway, R.E., Lin, J., Kennedy, M.W., Garside, P., Lawrence, C.E. & Ho, S.B. (2001) Coordinated Muc2 and Muc3 mucin gene expression in Trichinella spiralis infection in wild-type and cytokine-deficient mice. Digestive Diseases and Sciences 46, 17571764.Google Scholar
Siddhuraju, P. & Becker, K. (2003) Antioxidant properties of various solvent extracts of total phenolic constituents from three different agroclimatic origins of drumstick tree (Moringa oleifera Lam.). Journal of Agricultural and Food Chemistry 15, 21442155.Google Scholar
Singh, M.K., Paul, J., De, T. & Chakraborti, T. (2015) Bioactivity guided fractionation of Moringa oleifera Lam. flower targeting Leishmania donovani . Indian Journal of Experimental Biology 53, 747752.Google ScholarPubMed
Sinha, M., Das, D.K., Datta, S., Ghosh, S. & Dey, S. (2012) Amelioration of ionizing radiation induced lipid peroxidation in mouse liver by Moringa oleifera Lam. leaf extract. Indian Journal of Experimental Biology 50, 209215.Google ScholarPubMed
Skrzycki, M., Majewska, M., Podsiad, M., Czeczot, H., Salamatin, R., Twarowska, J. & Grytner-Zięcina, B. (2011) Hymenolepis diminuta: experimental studies on the antioxidant system with short and long term infection periods in the rats. Experimental Parasitology 129, 158163.CrossRefGoogle Scholar
Starke, W.A. & Oaks, J.A. (2001) Ileal mucosal mast cell, eosinophil, and goblet cell populations during Hymenolepis diminuta infection of the rat. Journal of Parasitology 87, 12221225.Google Scholar
Tsakiris, S., Schulpis, K.H., Marinou, M. & Behrakis, P. (2004) Protective effect of L-cysteine and glutathione on the modulated suckling rat brain Na+, K+, -ATPase and Mg2+-ATPase activities induced by the in vitro galactosaemia. Pharmacological Research 49, 475479.Google Scholar
Ugwu, O.P.C., Nwodo, O.F.C., Joshua, P.E., Odo, C.E., Bawa, A., Ossai, E.C. & Adonu, C.C. (2013) Anti-malaria and haematological analyses of ethanol leaf extract of Moringa oleifera on malaria infected mice. International Journal of Pharmacy and Biological Sciences 3, 360371.Google Scholar
Watanabe, N., Nawa, Y., Okamoto, K. & Kobayashi, A. (1994) Expulsion of Hymenolepis nana from mice with congenital deficiencies of IgE production or of mast cell development. Parasite Immunology 16, 137144.Google Scholar
Webb, R.A., Hoque, T. & Dimas, S. (2007) Expulsion of the gastrointestinal cestode, Hymenolepis diminuta by tolerant rats: evidence for mediation by a Th2 type immune enhanced goblet cell hyperplasia, increased mucin production and secretion. Parasite Immunology 29, 1121.Google Scholar
Willcocks, B., McAuliffe, G.N. & Baird, R.W. (2015) Dwarf tapeworm (Hymenolepis nana): characteristics in the Northern Territory 2002–2013. Journal of Paediatrics and Child Health 51, 982987.Google Scholar
Wright, S.H., Brown, J., Knight, P.A., Thornton, E.M., Kilshaw, P.J. & Miller, H.R. (2002) Transforming growth factor-beta1 mediates coexpression of the integrin subunit alphaE and the chymase mouse mast cell protease-1 during the early differentiation of bone marrow-derived mucosal mast cell homologues. Clinical and Experimental Allergy 32, 315324.Google Scholar